Experimental Estimation of Membrane Tension Induced by Osmotic Pressure

Osmotic pressure (Π) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions. However, there have been no experimental estimations of the membrane tension of vesicles upon exposure to Π. In this report, we estimated exp...

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Published in:Biophysical journal Vol. 111; no. 10; pp. 2190 - 2201
Main Authors: Alam Shibly, Sayed Ul, Ghatak, Chiranjib, Sayem Karal, Mohammad Abu, Moniruzzaman, Md, Yamazaki, Masahito
Format: Journal Article
Language:English
Published: United States Elsevier Inc 15-11-2016
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Abstract Osmotic pressure (Π) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions. However, there have been no experimental estimations of the membrane tension of vesicles upon exposure to Π. In this report, we estimated experimentally the lateral tension of the membranes of giant unilamellar vesicles (GUVs) when they were transferred into a hypotonic solution. First, we investigated the effect of Π on the rate constant, kp, of constant-tension (σex)-induced rupture of dioleoylphosphatidylcholine (DOPC)-GUVs using the method developed by us recently. We obtained the σex dependence of kp in GUVs under Π and by comparing this result with that in the absence of Π, we estimated the tension of the membrane due to Π at the swelling equilibrium, σosmeq. Next, we measured the volume change of DOPC-GUVs under small Π. The experimentally obtained values of σosmeq and the volume change agreed with their theoretical values within the limits of the experimental errors. Finally, we investigated the characteristics of the Π-induced pore formation in GUVs. The σosmeq corresponding to the threshold Π at which pore formation is induced is similar to the threshold tension of the σex-induced rupture. The time course of the radius change of GUVs in the Π-induced pore formation depends on the total membrane tension, σt; for small σt, the radius increased with time to an equilibrium one, which remained constant for a long time until pore formation, but for large σt, the radius increased with time and pore formation occurred before the swelling equilibrium was reached. Based on these results, we discussed the σosmeq and the Π-induced pore formation in lipid membranes.
AbstractList Osmotic pressure (Π) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions. However, there have been no experimental estimations of the membrane tension of vesicles upon exposure to Π. In this report, we estimated experimentally the lateral tension of the membranes of giant unilamellar vesicles (GUVs) when they were transferred into a hypotonic solution. First, we investigated the effect of Π on the rate constant, kp, of constant-tension (σex)-induced rupture of dioleoylphosphatidylcholine (DOPC)-GUVs using the method developed by us recently. We obtained the σex dependence of kp in GUVs under Π and by comparing this result with that in the absence of Π, we estimated the tension of the membrane due to Π at the swelling equilibrium, σosmeq. Next, we measured the volume change of DOPC-GUVs under small Π. The experimentally obtained values of σosmeq and the volume change agreed with their theoretical values within the limits of the experimental errors. Finally, we investigated the characteristics of the Π-induced pore formation in GUVs. The σosmeq corresponding to the threshold Π at which pore formation is induced is similar to the threshold tension of the σex-induced rupture. The time course of the radius change of GUVs in the Π-induced pore formation depends on the total membrane tension, σt; for small σt, the radius increased with time to an equilibrium one, which remained constant for a long time until pore formation, but for large σt, the radius increased with time and pore formation occurred before the swelling equilibrium was reached. Based on these results, we discussed the σosmeq and the Π-induced pore formation in lipid membranes.
Osmotic pressure (Π) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions. However, there have been no experimental estimations of the membrane tension of vesicles upon exposure to Π. In this report, we estimated experimentally the lateral tension of the membranes of giant unilamellar vesicles (GUVs) when they were transferred into a hypotonic solution. First, we investigated the effect of Π on the rate constant, k p , of constant-tension ( σ ex )-induced rupture of dioleoylphosphatidylcholine (DOPC)-GUVs using the method developed by us recently. We obtained the σ ex dependence of k p in GUVs under Π and by comparing this result with that in the absence of Π, we estimated the tension of the membrane due to Π at the swelling equilibrium, σ osm eq . Next, we measured the volume change of DOPC-GUVs under small Π. The experimentally obtained values of σ osm eq and the volume change agreed with their theoretical values within the limits of the experimental errors. Finally, we investigated the characteristics of the Π-induced pore formation in GUVs. The σ osm eq corresponding to the threshold Π at which pore formation is induced is similar to the threshold tension of the σ ex -induced rupture. The time course of the radius change of GUVs in the Π-induced pore formation depends on the total membrane tension, σ t ; for small σ t , the radius increased with time to an equilibrium one, which remained constant for a long time until pore formation, but for large σ t , the radius increased with time and pore formation occurred before the swelling equilibrium was reached. Based on these results, we discussed the σ osm eq and the Π-induced pore formation in lipid membranes.
Osmotic pressure (Π) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions. However, there have been no experimental estimations of the membrane tension of vesicles upon exposure to Π. In this report, we estimated experimentally the lateral tension of the membranes of giant unilamellar vesicles (GUVs) when they were transferred into a hypotonic solution. First, we investigated the effect of Π on the rate constant, k , of constant-tension (σ )-induced rupture of dioleoylphosphatidylcholine (DOPC)-GUVs using the method developed by us recently. We obtained the σ dependence of k in GUVs under Π and by comparing this result with that in the absence of Π, we estimated the tension of the membrane due to Π at the swelling equilibrium, σ . Next, we measured the volume change of DOPC-GUVs under small Π. The experimentally obtained values of σ and the volume change agreed with their theoretical values within the limits of the experimental errors. Finally, we investigated the characteristics of the Π-induced pore formation in GUVs. The σ corresponding to the threshold Π at which pore formation is induced is similar to the threshold tension of the σ -induced rupture. The time course of the radius change of GUVs in the Π-induced pore formation depends on the total membrane tension, σ ; for small σ , the radius increased with time to an equilibrium one, which remained constant for a long time until pore formation, but for large σ , the radius increased with time and pore formation occurred before the swelling equilibrium was reached. Based on these results, we discussed the σ and the Π-induced pore formation in lipid membranes.
Osmotic pressure (...) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions. However, there have been no experimental estimations of the membrane tension of vesicles upon exposure to ... In this report, we estimated experimentally the lateral tension of the membranes of giant unilamellar vesicles (GUVs) when they were transferred into a hypotonic solution. First, we investigated the effect of ... on the rate constant, kp, of constant-tension (sex)-induced rupture of dioleoylphosphatidylcholine (DOPC)-GUVs using the method developed by us recently. We obtained the sex dependence of kp in GUVs under ... and by comparing this result with that in the absence of ..., we estimated the tension of the membrane due to ... at the swelling equilibrium, Math Eq. Next, we measured the volume change of DOPC-GUVs under small ... The experimentally obtained values of Math Eq and the volume change agreed with their theoretical values within the limits of the experimental errors. Finally, we investigated the characteristics of the ...-induced pore formation in GUVs. The Math Eq corresponding to the threshold ... at which pore formation is induced is similar to the threshold tension of the sex-induced rupture. The time course of the radius change of GUVs in the ...-induced pore formation depends on the total membrane tension, st; for small st, the radius increased with time to an equilibrium one, which remained constant for a long time until pore formation, but for large st, the radius increased with time and pore formation occurred before the swelling equilibrium was reached. Based on these results, we discussed the Math Eq and the ...-induced pore formation in lipid membranes. (ProQuest: ... denotes formulae/symbols omitted.)
Author Moniruzzaman, Md
Yamazaki, Masahito
Sayem Karal, Mohammad Abu
Alam Shibly, Sayed Ul
Ghatak, Chiranjib
AuthorAffiliation 1 Integrated Bioscience Section, Graduate School of Science and Technology, Shizuoka University, Shizuoka, Japan
3 Department of Physics, Faculty of Science, Shizuoka University, Shizuoka, Japan
2 Nanomaterials Research Division, Research Institute of Electronics, Shizuoka University, Shizuoka, Japan
AuthorAffiliation_xml – name: 2 Nanomaterials Research Division, Research Institute of Electronics, Shizuoka University, Shizuoka, Japan
– name: 3 Department of Physics, Faculty of Science, Shizuoka University, Shizuoka, Japan
– name: 1 Integrated Bioscience Section, Graduate School of Science and Technology, Shizuoka University, Shizuoka, Japan
Author_xml – sequence: 1
  givenname: Sayed Ul
  surname: Alam Shibly
  fullname: Alam Shibly, Sayed Ul
  organization: Integrated Bioscience Section, Graduate School of Science and Technology, Shizuoka University, Shizuoka, Japan
– sequence: 2
  givenname: Chiranjib
  surname: Ghatak
  fullname: Ghatak, Chiranjib
  organization: Nanomaterials Research Division, Research Institute of Electronics, Shizuoka University, Shizuoka, Japan
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  givenname: Mohammad Abu
  surname: Sayem Karal
  fullname: Sayem Karal, Mohammad Abu
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  surname: Yamazaki
  fullname: Yamazaki, Masahito
  email: yamazaki.masahito@shizuoka.ac.jp
  organization: Integrated Bioscience Section, Graduate School of Science and Technology, Shizuoka University, Shizuoka, Japan
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27851942$$D View this record in MEDLINE/PubMed
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Snippet Osmotic pressure (Π) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions....
Osmotic pressure (...) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological...
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SourceType Open Access Repository
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StartPage 2190
SubjectTerms Biophysics
Cell Membrane - chemistry
Cell Membrane - metabolism
Cells
Kinetics
Lipids
Membranes
Osmotic Pressure
Phosphatidylcholines - chemistry
Sucrose - metabolism
Unilamellar Liposomes - chemistry
Unilamellar Liposomes - metabolism
Title Experimental Estimation of Membrane Tension Induced by Osmotic Pressure
URI https://dx.doi.org/10.1016/j.bpj.2016.09.043
https://www.ncbi.nlm.nih.gov/pubmed/27851942
https://www.proquest.com/docview/1843266179
https://search.proquest.com/docview/1841133222
https://pubmed.ncbi.nlm.nih.gov/PMC5112947
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