How cholesterol stiffens unsaturated lipid membranes

Cholesterol is an integral component of eukaryotic cell membranes and a key molecule in controlling membrane fluidity, organization, and other physicochemical parameters. It also plays a regulatory function in antibiotic drug resistance and the immune response of cells against viruses, by stabilizin...

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Vydané v:Proceedings of the National Academy of Sciences - PNAS Ročník 117; číslo 36; s. 21896
Hlavní autori: Chakraborty, Saptarshi, Doktorova, Milka, Molugu, Trivikram R, Heberle, Frederick A, Scott, Haden L, Dzikovski, Boris, Nagao, Michihiro, Stingaciu, Laura-Roxana, Standaert, Robert F, Barrera, Francisco N, Katsaras, John, Khelashvili, George, Brown, Michael F, Ashkar, Rana
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States 08.09.2020
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ISSN:1091-6490, 1091-6490
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Abstract Cholesterol is an integral component of eukaryotic cell membranes and a key molecule in controlling membrane fluidity, organization, and other physicochemical parameters. It also plays a regulatory function in antibiotic drug resistance and the immune response of cells against viruses, by stabilizing the membrane against structural damage. While it is well understood that, structurally, cholesterol exhibits a densification effect on fluid lipid membranes, its effects on membrane bending rigidity are assumed to be nonuniversal; i.e., cholesterol stiffens saturated lipid membranes, but has no stiffening effect on membranes populated by unsaturated lipids, such as 1,2-dioleoyl- -glycero-3-phosphocholine (DOPC). This observation presents a clear challenge to structure-property relationships and to our understanding of cholesterol-mediated biological functions. Here, using a comprehensive approach-combining neutron spin-echo (NSE) spectroscopy, solid-state deuterium NMR ( H NMR) spectroscopy, and molecular dynamics (MD) simulations-we report that cholesterol locally increases the bending rigidity of DOPC membranes, similar to saturated membranes, by increasing the bilayer's packing density. All three techniques, inherently sensitive to mesoscale bending fluctuations, show up to a threefold increase in effective bending rigidity with increasing cholesterol content approaching a mole fraction of 50%. Our observations are in good agreement with the known effects of cholesterol on the area-compressibility modulus and membrane structure, reaffirming membrane structure-property relationships. The current findings point to a scale-dependent manifestation of membrane properties, highlighting the need to reassess cholesterol's role in controlling membrane bending rigidity over mesoscopic length and time scales of important biological functions, such as viral budding and lipid-protein interactions.
AbstractList Cholesterol is an integral component of eukaryotic cell membranes and a key molecule in controlling membrane fluidity, organization, and other physicochemical parameters. It also plays a regulatory function in antibiotic drug resistance and the immune response of cells against viruses, by stabilizing the membrane against structural damage. While it is well understood that, structurally, cholesterol exhibits a densification effect on fluid lipid membranes, its effects on membrane bending rigidity are assumed to be nonuniversal; i.e., cholesterol stiffens saturated lipid membranes, but has no stiffening effect on membranes populated by unsaturated lipids, such as 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC). This observation presents a clear challenge to structure-property relationships and to our understanding of cholesterol-mediated biological functions. Here, using a comprehensive approach-combining neutron spin-echo (NSE) spectroscopy, solid-state deuterium NMR (2H NMR) spectroscopy, and molecular dynamics (MD) simulations-we report that cholesterol locally increases the bending rigidity of DOPC membranes, similar to saturated membranes, by increasing the bilayer's packing density. All three techniques, inherently sensitive to mesoscale bending fluctuations, show up to a threefold increase in effective bending rigidity with increasing cholesterol content approaching a mole fraction of 50%. Our observations are in good agreement with the known effects of cholesterol on the area-compressibility modulus and membrane structure, reaffirming membrane structure-property relationships. The current findings point to a scale-dependent manifestation of membrane properties, highlighting the need to reassess cholesterol's role in controlling membrane bending rigidity over mesoscopic length and time scales of important biological functions, such as viral budding and lipid-protein interactions.Cholesterol is an integral component of eukaryotic cell membranes and a key molecule in controlling membrane fluidity, organization, and other physicochemical parameters. It also plays a regulatory function in antibiotic drug resistance and the immune response of cells against viruses, by stabilizing the membrane against structural damage. While it is well understood that, structurally, cholesterol exhibits a densification effect on fluid lipid membranes, its effects on membrane bending rigidity are assumed to be nonuniversal; i.e., cholesterol stiffens saturated lipid membranes, but has no stiffening effect on membranes populated by unsaturated lipids, such as 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC). This observation presents a clear challenge to structure-property relationships and to our understanding of cholesterol-mediated biological functions. Here, using a comprehensive approach-combining neutron spin-echo (NSE) spectroscopy, solid-state deuterium NMR (2H NMR) spectroscopy, and molecular dynamics (MD) simulations-we report that cholesterol locally increases the bending rigidity of DOPC membranes, similar to saturated membranes, by increasing the bilayer's packing density. All three techniques, inherently sensitive to mesoscale bending fluctuations, show up to a threefold increase in effective bending rigidity with increasing cholesterol content approaching a mole fraction of 50%. Our observations are in good agreement with the known effects of cholesterol on the area-compressibility modulus and membrane structure, reaffirming membrane structure-property relationships. The current findings point to a scale-dependent manifestation of membrane properties, highlighting the need to reassess cholesterol's role in controlling membrane bending rigidity over mesoscopic length and time scales of important biological functions, such as viral budding and lipid-protein interactions.
Cholesterol is an integral component of eukaryotic cell membranes and a key molecule in controlling membrane fluidity, organization, and other physicochemical parameters. It also plays a regulatory function in antibiotic drug resistance and the immune response of cells against viruses, by stabilizing the membrane against structural damage. While it is well understood that, structurally, cholesterol exhibits a densification effect on fluid lipid membranes, its effects on membrane bending rigidity are assumed to be nonuniversal; i.e., cholesterol stiffens saturated lipid membranes, but has no stiffening effect on membranes populated by unsaturated lipids, such as 1,2-dioleoyl- -glycero-3-phosphocholine (DOPC). This observation presents a clear challenge to structure-property relationships and to our understanding of cholesterol-mediated biological functions. Here, using a comprehensive approach-combining neutron spin-echo (NSE) spectroscopy, solid-state deuterium NMR ( H NMR) spectroscopy, and molecular dynamics (MD) simulations-we report that cholesterol locally increases the bending rigidity of DOPC membranes, similar to saturated membranes, by increasing the bilayer's packing density. All three techniques, inherently sensitive to mesoscale bending fluctuations, show up to a threefold increase in effective bending rigidity with increasing cholesterol content approaching a mole fraction of 50%. Our observations are in good agreement with the known effects of cholesterol on the area-compressibility modulus and membrane structure, reaffirming membrane structure-property relationships. The current findings point to a scale-dependent manifestation of membrane properties, highlighting the need to reassess cholesterol's role in controlling membrane bending rigidity over mesoscopic length and time scales of important biological functions, such as viral budding and lipid-protein interactions.
Author Ashkar, Rana
Standaert, Robert F
Khelashvili, George
Barrera, Francisco N
Doktorova, Milka
Brown, Michael F
Scott, Haden L
Molugu, Trivikram R
Nagao, Michihiro
Stingaciu, Laura-Roxana
Katsaras, John
Chakraborty, Saptarshi
Dzikovski, Boris
Heberle, Frederick A
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  organization: Center for Soft Matter and Biological Physics, Virginia Tech, Blacksburg, VA 24061
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  givenname: Milka
  orcidid: 0000-0003-4366-2242
  surname: Doktorova
  fullname: Doktorova, Milka
  organization: Department of Integrative Biology and Pharmacology, University of Texas Health Science Center, Houston, TX 77030
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  givenname: Trivikram R
  orcidid: 0000-0002-3254-0445
  surname: Molugu
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  organization: Department of Chemistry and Biochemistry, University of Arizona, Tucson, AZ 85721
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  surname: Heberle
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  organization: Bredesen Center, University of Tennessee, Knoxville, TN 37996
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  organization: Center for Environmental Biotechnology, University of Tennessee, Knoxville, TN 37920
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  surname: Dzikovski
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  organization: ACERT, National Biomedical Center for Advanced ESR Technology, Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853
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  orcidid: 0000-0003-3617-251X
  surname: Nagao
  fullname: Nagao, Michihiro
  organization: Center for Exploration of Energy and Matter, Department of Physics, Indiana University, Bloomington, IN 47408
– sequence: 8
  givenname: Laura-Roxana
  surname: Stingaciu
  fullname: Stingaciu, Laura-Roxana
  organization: Neutron Scattering Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831
– sequence: 9
  givenname: Robert F
  surname: Standaert
  fullname: Standaert, Robert F
  organization: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831
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  givenname: Francisco N
  orcidid: 0000-0002-5200-7891
  surname: Barrera
  fullname: Barrera, Francisco N
  organization: Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, TN 37996
– sequence: 11
  givenname: John
  orcidid: 0000-0002-8937-4177
  surname: Katsaras
  fullname: Katsaras, John
  organization: Shull Wollan Center, Oak Ridge National Laboratory, Oak Ridge, TN 37831
– sequence: 12
  givenname: George
  orcidid: 0000-0001-7235-8579
  surname: Khelashvili
  fullname: Khelashvili, George
  organization: Institute of Computational Biomedicine, Weill Cornell Medical College, New York, NY 10065
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  orcidid: 0000-0003-4154-0241
  surname: Brown
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  email: ashkar@vt.edu, mfbrown@u.arizona.edu
  organization: Department of Chemistry and Biochemistry, University of Arizona, Tucson, AZ 85721; ashkar@vt.edu mfbrown@u.arizona.edu
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  organization: Center for Soft Matter and Biological Physics, Virginia Tech, Blacksburg, VA 24061
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32843347$$D View this record in MEDLINE/PubMed
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Keywords molecular dynamics simulations
membrane viscosity
deuterium NMR
area compressibility
neutron spin echo
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PublicationTitle Proceedings of the National Academy of Sciences - PNAS
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Snippet Cholesterol is an integral component of eukaryotic cell membranes and a key molecule in controlling membrane fluidity, organization, and other physicochemical...
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SubjectTerms Biomechanical Phenomena
Cell Membrane - chemistry
Cell Membrane - metabolism
Cholesterol - chemistry
Cholesterol - metabolism
Magnetic Resonance Spectroscopy
Membrane Fluidity
Membrane Lipids - chemistry
Membrane Lipids - metabolism
Molecular Dynamics Simulation
Title How cholesterol stiffens unsaturated lipid membranes
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