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: | , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
United States
08.09.2020
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| Predmet: | |
| 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 |
| Author_xml | – sequence: 1 givenname: Saptarshi surname: Chakraborty fullname: Chakraborty, Saptarshi organization: Center for Soft Matter and Biological Physics, Virginia Tech, Blacksburg, VA 24061 – sequence: 2 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 – sequence: 3 givenname: Trivikram R orcidid: 0000-0002-3254-0445 surname: Molugu fullname: Molugu, Trivikram R organization: Department of Chemistry and Biochemistry, University of Arizona, Tucson, AZ 85721 – sequence: 4 givenname: Frederick A orcidid: 0000-0002-0424-3240 surname: Heberle fullname: Heberle, Frederick A organization: Bredesen Center, University of Tennessee, Knoxville, TN 37996 – sequence: 5 givenname: Haden L surname: Scott fullname: Scott, Haden L organization: Center for Environmental Biotechnology, University of Tennessee, Knoxville, TN 37920 – sequence: 6 givenname: Boris surname: Dzikovski fullname: Dzikovski, Boris organization: ACERT, National Biomedical Center for Advanced ESR Technology, Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853 – sequence: 7 givenname: Michihiro 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 – sequence: 10 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 – sequence: 13 givenname: Michael F orcidid: 0000-0003-4154-0241 surname: Brown fullname: Brown, Michael F 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 – sequence: 14 givenname: Rana orcidid: 0000-0003-4075-2330 surname: Ashkar fullname: Ashkar, Rana email: ashkar@vt.edu, mfbrown@u.arizona.edu 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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| 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 |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/32843347 https://www.proquest.com/docview/2437401012 |
| Volume | 117 |
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