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
Main Authors: Kosmalska, Anita Joanna, Casares, Laura, Elosegui-Artola, Alberto, Thottacherry, Joseph Jose, Moreno-Vicente, Roberto, González-Tarragó, Víctor, del Pozo, Miguel Ángel, Mayor, Satyajit, Arroyo, Marino, Navajas, Daniel, Trepat, Xavier, Gauthier, Nils C., Roca-Cusachs, Pere
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Published: London Nature Publishing Group UK 15-06-2015
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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.
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.
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  organization: Institute for Bioengineering of Catalonia (IBEC), Department of Physiological Sciences I, University of Barcelona
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  organization: Institute for Bioengineering of Catalonia (IBEC)
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  organization: National Centre for Biological Sciences (TIFR)
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  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
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  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)
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  givenname: Nils C.
  surname: Gauthier
  fullname: Gauthier, Nils C.
  email: mbinclg@nus.edu.sg
  organization: Mechanobiology Institute, National University of Singapore
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  surname: Roca-Cusachs
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26073653$$D View this record in MEDLINE/PubMed
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Universitat Politècnica de Catalunya. LACÀN - Mètodes Numèrics en Ciències Aplicades i Enginyeria
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Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. 2015 Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.
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SSID ssj0000391844
Score 2.5044587
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...
SourceID pubmedcentral
csuc
proquest
crossref
pubmed
springer
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 7292
SubjectTerms 13/109
14/19
631/57/2271
631/57/2272/2275
631/80/642
92 Biology and other natural sciences
92B Mathematical biology in general
Adaptation, Physiological - physiology
ALVEOLAR EPITHELIAL-CELLS
Animals
Biologia
Biomathematics
Cell Membrane - physiology
Cell Shape
Cell Size
Classificació AMS
DYNAMICS
Elasticity
EXOCYTOSIS
Fibroblasts - physiology
Humanities and Social Sciences
LIVING CELLS
Matemàtica aplicada a les ciències
Matemàtiques i estadística
Mice
MIGRATION
Models matemàtics
Models, Biological
Models, Theoretical
multidisciplinary
NEURONS
Osmolar Concentration
Physiology
Science
Science (multidisciplinary)
SHAPE
STRESS
Stress, Mechanical
SURFACE-AREA REGULATION
TENSION
Àrees temàtiques de la UPC
Title Physical principles of membrane remodelling during cell mechanoadaptation
URI https://link.springer.com/article/10.1038/ncomms8292
https://www.ncbi.nlm.nih.gov/pubmed/26073653
https://www.proquest.com/docview/1687997627
https://search.proquest.com/docview/1689309069
https://recercat.cat/handle/2072/291126
https://pubmed.ncbi.nlm.nih.gov/PMC4490354
Volume 6
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