Physical principles of membrane remodelling during cell mechanoadaptation
Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope—the bilayer membrane. However, the fundamental biophysical principles by which the cell membrane allows for and responds to shape changes remain unclear. Here we...
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Published in: | Nature communications Vol. 6; no. 1; p. 7292 |
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Abstract | Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope—the bilayer membrane. However, the fundamental biophysical principles by which the cell membrane allows for and responds to shape changes remain unclear. Here we show that the 3D remodelling of the membrane in response to a broad diversity of physiological perturbations can be explained by a purely mechanical process. This process is passive, local, almost instantaneous, before any active remodelling and generates different types of membrane invaginations that can repeatedly store and release large fractions of the cell membrane. We further demonstrate that the shape of those invaginations is determined by the minimum elastic and adhesive energy required to store both membrane area and liquid volume at the cell–substrate interface. Once formed, cells reabsorb the invaginations through an active process with duration of the order of minutes.
Variations in cell shape must be accommodated by the cell membrane, but how the membrane adjusts to changes in area and volume is not known. Here the authors show that the membrane responds in a nearly instantaneous, purely physical manner involving the flattening or generation of membrane invaginations. |
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AbstractList | Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope--the bilayer membrane. However, the fundamental biophysical principles by which the cell membrane allows for and responds to shape changes remain unclear. Here we show that the 3D remodelling of the membrane in response to a broad diversity of physiological perturbations can be explained by a purely mechanical process. This process is passive, local, almost instantaneous, before any active remodelling and generates different types of membrane invaginations that can repeatedly store and release large fractions of the cell membrane. We further demonstrate that the shape of those invaginations is determined by the minimum elastic and adhesive energy required to store both membrane area and liquid volume at the cell-substrate interface. Once formed, cells reabsorb the invaginations through an active process with duration of the order of minutes. Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope—the bilayer membrane. However, the fundamental biophysical principles by which the cell membrane allows for and responds to shape changes remain unclear. Here we show that the 3D remodelling of the membrane in response to a broad diversity of physiological perturbations can be explained by a purely mechanical process. This process is passive, local, almost instantaneous, before any active remodelling and generates different types of membrane invaginations that can repeatedly store and release large fractions of the cell membrane. We further demonstrate that the shape of those invaginations is determined by the minimum elastic and adhesive energy required to store both membrane area and liquid volume at the cell–substrate interface. Once formed, cells reabsorb the invaginations through an active process with duration of the order of minutes. Variations in cell shape must be accommodated by the cell membrane, but how the membrane adjusts to changes in area and volume is not known. Here the authors show that the membrane responds in a nearly instantaneous, purely physical manner involving the flattening or generation of membrane invaginations. Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope-the bilayer membrane. However, the fundamental biophysical principles by which the cell membrane allows for and responds to shape changes remain unclear. Here we show that the 3D remodelling of the membrane in response to a broad diversity of physiological perturbations can be explained by a purely mechanical process. This process is passive, local, almost instantaneous, before any active remodelling and generates different types of membrane invaginations that can repeatedly store and release large fractions of the cell membrane. We further demonstrate that the shape of those invaginations is determined by the minimum elastic and adhesive energy required to store both membrane area and liquid volume at the cell-substrate interface. Once formed, cells reabsorb the invaginations through an active process with duration of the order of minutes. Peer Reviewed |
ArticleNumber | 7292 |
Author | Kosmalska, Anita Joanna Elosegui-Artola, Alberto Roca-Cusachs, Pere González-Tarragó, Víctor Mayor, Satyajit Casares, Laura Thottacherry, Joseph Jose del Pozo, Miguel Ángel Trepat, Xavier Arroyo, Marino Moreno-Vicente, Roberto Navajas, Daniel Gauthier, Nils C. |
Author_xml | – sequence: 1 givenname: Anita Joanna surname: Kosmalska fullname: Kosmalska, Anita Joanna organization: Institute for Bioengineering of Catalonia (IBEC), Department of Physiological Sciences I, University of Barcelona – sequence: 2 givenname: Laura surname: Casares fullname: Casares, Laura organization: Institute for Bioengineering of Catalonia (IBEC), Department of Physiological Sciences I, University of Barcelona – sequence: 3 givenname: Alberto surname: Elosegui-Artola fullname: Elosegui-Artola, Alberto organization: Institute for Bioengineering of Catalonia (IBEC) – sequence: 4 givenname: Joseph Jose surname: Thottacherry fullname: Thottacherry, Joseph Jose organization: National Centre for Biological Sciences (TIFR) – sequence: 5 givenname: Roberto surname: Moreno-Vicente fullname: Moreno-Vicente, Roberto organization: Centro Nacional de Investigaciones Cardiovasculares (CNIC) – sequence: 6 givenname: Víctor surname: González-Tarragó fullname: González-Tarragó, Víctor organization: Institute for Bioengineering of Catalonia (IBEC), Department of Physiological Sciences I, University of Barcelona – sequence: 7 givenname: Miguel Ángel surname: del Pozo fullname: del Pozo, Miguel Ángel organization: Centro Nacional de Investigaciones Cardiovasculares (CNIC) – sequence: 8 givenname: Satyajit surname: Mayor fullname: Mayor, Satyajit organization: National Centre for Biological Sciences (TIFR) – sequence: 9 givenname: Marino orcidid: 0000-0003-1647-940X surname: Arroyo fullname: Arroyo, Marino organization: LaCàN, Universitat Politècnica de Catalunya-BarcelonaTech – sequence: 10 givenname: Daniel surname: Navajas fullname: Navajas, Daniel organization: Institute for Bioengineering of Catalonia (IBEC), Department of Physiological Sciences I, University of Barcelona, Ciber Enfermedades Respiratorias – sequence: 11 givenname: Xavier surname: Trepat fullname: Trepat, Xavier organization: Institute for Bioengineering of Catalonia (IBEC), Department of Physiological Sciences I, University of Barcelona, Institució Catalana de Recerca i Estudis Avançats (ICREA) – sequence: 12 givenname: Nils C. surname: Gauthier fullname: Gauthier, Nils C. email: mbinclg@nus.edu.sg organization: Mechanobiology Institute, National University of Singapore – sequence: 13 givenname: Pere surname: Roca-Cusachs fullname: Roca-Cusachs, Pere email: rocacusachs@ub.edu organization: Institute for Bioengineering of Catalonia (IBEC), Department of Physiological Sciences I, University of Barcelona |
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Snippet | Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope—the bilayer... Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope--the bilayer... Biological processes in any physiological environment involve changes in cell shape, which must be accommodated by their physical envelope-the bilayer... |
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Title | Physical principles of membrane remodelling during cell mechanoadaptation |
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