Molecular structures of fluid phosphatidylethanolamine bilayers obtained from simulation-to-experiment comparisons and experimental scattering density profiles

Journal of Physical Chemistry A

Volumn 119, Issue 5, 2015, Pages 1947-1956

  Kučerka, Norbert ^a,b,c   Van Oosten, Brad ^d   Pan, Jianjun ^e,f   Heberle, Frederick A ^f   Harroun, Thad A ^d   Katsaras, John ^f,g  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b Physics and Informatics   (Slovakia)

^c JOINT INSTITUTE FOR NUCLEAR RESEARCH   (Russian Federation)

^d BROCK UNIVERSITY   (Canada)

^e UNIVERSITY OF SOUTH FLORIDA   (United States)

^f OAK RIDGE NATIONAL LABORATORY   (United States)

^g UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDRATION; HYDROCARBONS; HYDROGEN BONDS;

CHANGING TEMPERATURE; GLYCEROL BACKBONE; HYDROCARBON CHAINS; PHOSPHATIDYLETHANOLAMINE; SCATTERING DENSITY; SCATTERING MEASUREMENTS; STRUCTURAL PARAMETER; TEMPERATURE CHANGES;

LIPID BILAYERS;

LIPID BILAYER; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE;

CHEMISTRY; LIPID BILAYER; MOLECULAR DYNAMICS; NEUTRON DIFFRACTION; SMALL ANGLE SCATTERING; X RAY DIFFRACTION;

LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; NEUTRON DIFFRACTION; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLSERINES; SCATTERING, SMALL ANGLE; X-RAY DIFFRACTION;

EID: 84922440734     PISSN: 10895639     EISSN: 15205215     Source Type: Journal    
DOI: 10.1021/jp511159q     Document Type: Article

References (74)

1. Harroun, T. A.; Kučerka, N.; Nieh, M. P.; Katsaras, J. Neutron and X-Ray Scattering for Biophysics and Biotechnology: Examples of Self-Assembled Lipid Systems Soft Matter 2009, 5, 2694-2703
2. Cullis, P. R.; Hope, M. J. Biochemistry of Lipids and Membranes; The Benjamin/Cumings Publishing Company, Inc.: Menlo Park, CA, 1985; Chapter 2, pp 25-72.
3. van Meer, G.; Voelker, D. R.; Feigenson, G. W. Membrane Lipids: Where They Are and How They Behave Nat. Rev. Mol. Cell Biol. 2008, 9, 112-124
4. Marsh, D. Handbook of Lipid Bilayers, 2nd ed.; CRC Press: Boca Raton, 2013.
5. Marsh, D. Lateral Pressure Profile, Spontaneous Curvature Frustration, and the Incorporation and Conformation of Proteins in Membranes Biophys. J. 2007, 93, 3884-3899
6. Pabst, G.; Kučerka, N.; Nieh, M. P.; Rheinstädter, M. C.; Katsaras, J. Applications of Neutron and X-Ray Scattering to the Study of Biologically Relevant Model Membranes Chem. Phys. Lipids 2010, 163, 460-479
7. Kučerka, N.; Nieh, M. P.; Pencer, J.; Harroun, T. A.; Katsaras, J. The Study of Liposomes, Lamellae and Membranes Using Neutrons and X-Rays Curr. Opin. Colloid Interface Sci. 2007, 12, 17-22
8. Weijers, R. N. Lipid Composition of Cell Membranes and Its Relevance in Type 2 Diabetes Mellitus Curr. Diabetes Rev. 2012, 8, 390-400
9. Vance, J. E.; Tasseva, G. Formation and Function of Phosphatidylserine and Phosphatidylethanolamine in Mammalian Cells Biochim. Biophys. Acta 2013, 1831, 543-554
10. Vance, J. E. Thematic Review Series: Glycerolipids. Phosphatidylserine and Phosphatidylethanolamine in Mammalian Cells: Two Metabolically Related Aminophospholipids J. Lipid Res. 2008, 49, 1377-1387
11. Li, Z.; Agellon, L. B.; Allen, T. M.; Umeda, M.; Jewell, L.; Mason, A.; Vance, D. E. The Ratio of Phosphatidylcholine to Phosphatidylethanolamine Influences Membrane Integrity and Steatohepatitis Cell Metab. 2006, 3, 321-331
12. Post, J. A.; Bijvelt, J. J.; Verkleij, A. J. Phosphatidylethanolamine and Sarcolemmal Damage During Ischemia or Metabolic Inhibition of Heart Myocytes Am. J. Physiol. 1995, 268, H773-H780
13. Tasseva, G.; Bai, H. D.; Davidescu, M.; Haromy, A.; Michelakis, E.; Vance, J. E. Phosphatidylethanolamine Deficiency in Mammalian Mitochondria Impairs Oxidative Phosphorylation and Alters Mitochondrial Morphology J. Biol. Chem. 2013, 288, 4158-4173
14. Johri, A.; Beal, M. F. Mitochondrial Dysfunction in Neurodegenerative Diseases J. Pharmacol. Exp. Therapeutics 2012, 342, 619-630
15. Ren, J.; Pulakat, L.; Whaley-Connell, A.; Sowers, J. R. Mitochondrial Biogenesis in the Metabolic Syndrome and Cardiovascular Disease J. Mol. Med. (Berlin) 2010, 88, 993-1001
16. Supale, S.; Li, N.; Brun, T.; Maechler, P. Mitochondrial Dysfunction in Pancreatic Beta Cells Trends Endocrinol. Metab. 2012, 23, 477-487
17. Baysal, B. E.; Ferrell, R. E.; Willett-Brozick, J. E.; Lawrence, E. C.; Myssiorek, D.; Bosch, A.; van der, M. A.; Taschner, P. E.; Rubinstein, W. S.; Myers, E. N.; Richard, C. W., III; Cornelisse, C. J.; Devilee, P.; Devlin, B. Mutations in SDHD, a Mitochondrial Complex II Gene, in Hereditary Paraganglioma Science 2000, 287, 848-851
18. Goldfine, H. Lipid Chemistry and Metabolism Annu. Rev. Biochem. 1968, 37, 303-330
19. Heberle, F. A.; Pan, J.; Standaert, R. F.; Drazba, P.; Kučerka, N.; Katsaras, J. Model-Based Approaches for the Determination of Lipid Bilayer Structure From Small-Angle Neutron and X-Ray Scattering Data Eur. Biophys. J. 2012, 41, 875-890
20. Kučerka, N.; Nagle, J. F.; Sachs, J. N.; Feller, S. E.; Pencer, J.; Jackson, A.; Katsaras, J. Lipid Bilayer Structure Determined by the Simultaneous Analysis of Neutron and X-Ray Scattering Data Biophys. J. 2008, 95, 2356-2367
21. Kučerka, N.; Katsaras, J.; Nagle, J. F. Comparing Membrane Simulations to Scattering Experiments: Introducing the SIMtoEXP Software J. Membr. Biol. 2010, 235, 43-50
22. Bhatnagar, N.; Kamath, G.; Potoff, J. J. Biomolecular Simulations With the Transferable Potentials for Phase Equilibria: Extension to Phospholipids J. Phys. Chem. B 2013, 117, 9910-9921
23. Braun, A. R.; Sachs, J. N.; Nagle, J. F. Comparing Simulations of Lipid Bilayers to Scattering Data: the GROMOS 43A1-S3 Force Field J. Phys. Chem. B 2013, 117, 5065-5072
24. Dickson, C. J.; Madej, B. D.; Skjevik, A. A.; Betz, R. M.; Teigen, K.; Gould, I. R.; Walker, R. C. Lipid14: The Amber Lipid Force Field J. Chem. Theory Comput. 2014, 10, 865-879
25. Jämbeck, J. P. M.; Lyubartsev, A. P. An Extension and Further Validation of an All-Atomistic Force Field for Biological Membranes J. Chem. Theory Comput. 2012, 8, 2938-2948
26. Jämbeck, J. P. M.; Lyubartsev, A. P. Derivation and Systematic Validation of a Refined All-Atom Force Field for Phosphatidylcholine Lipids J. Phys. Chem. B 2012, 116, 3164-3179
27. Jämbeck, J. P. M.; Lyubartsev, A. P. Another Piece of the Membrane Puzzle: Extending Slipids Further J. Chem. Theory Comput. 2012, 9, 774-784
28. Lee, S.; Tran, A.; Allsopp, M.; Lim, J. B.; Henin, J.; Klauda, J. B. CHARMM36 United Atom Chain Model for Lipids and Surfactants J. Phys. Chem. B 2014, 118, 547-556
29. Nagle, J. F. Introductory Lecture: Basic Quantities in Model Biomembranes Faraday Discuss. 2013, 161, 11-29
30. Raghunathan, M.; Zubovski, Y.; Venable, R. M.; Pastor, R. W.; Nagle, J. F.; Tristram-Nagle, S. Structure and Elasticity of Lipid Membranes With Genistein and Daidzein Bioflavinoids Using X-Ray Scattering and MD Simulations J. Phys. Chem. B 2012, 116, 3918-3927
31. Zhuang, X.; Makover, J. R.; Im, W.; Klauda, J. B. A Systematic Molecular Dynamics Simulation Study of Temperature Dependent Bilayer Structural Properties Biochim. Biophys. Acta 2014, 1838, 2520-2529
32. Kučerka, N.; Nieh, M. P.; Katsaras, J. Fluid Phase Lipid Areas and Bilayer Thicknesses of Commonly Used Phosphatidylcholines As a Function of Temperature Biochim. Biophys. Acta 2011, 1808, 2761-2771
33. Pan, J.; Cheng, X.; Heberle, F. A.; Mostofian, B.; Kučerka, N.; Drazba, P.; Katsaras, J. Interactions Between Ether Phospholipids and Cholesterol As Determined by Scattering and Molecular Dynamics Simulations J. Phys. Chem. B 2012, 116, 14829-14838
34. Pan, J.; Heberle, F. A.; Tristram-Nagle, S.; Szymanski, M.; Koepfinger, M.; Katsaras, J.; Kučerka, N. Molecular Structures of Fluid Phase Phosphatidylglycerol Bilayers As Determined by Small Angle Neutron and X-Ray Scattering Biochim. Biophys. Acta 2012, 1818, 2135-2148
35. Pan, J.; Marquardt, D.; Heberle, F. A.; Kučerka, N.; Katsaras, J. Revisiting the Bilayer Structures of Fluid Phase Phosphatidylglycerol Lipids: Accounting for Exchangeable Hydrogens Biochim. Biophys. Acta 2014, 1838, 2966-2969
36. Pan, J.; Cheng, X.; Monticelli, L.; Heberle, F. A.; Kučerka, N.; Tieleman, D. P.; Katsaras, J. The Molecular Structure of a Phosphatidylserine Bilayer Determined by Scattering and Molecular Dynamics Simulations Soft Matter 2014, 10, 3716-3725
37. Kučerka, N.; Pencer, J.; Sachs, J. N.; Nagle, J. F.; Katsaras, J. Curvature Effect on the Structure of Phospholipid Bilayers Langmuir 2007, 23, 1292-1299
38. Heller, W. T.; Lynn, G. W.; Urban, V. S.; Weiss, K.; Myles, D. A. A. The Bio-SANS Small-Angle Neutron Scattering Instrument at Oak Ridge National Laboratory Neutron News 2008, 19, 22-23
39. Kučerka, N.; Liu, Y.; Chu, N.; Petrache, H. I.; Tristram-Nagle, S.; Nagle, J. F. Structure of Fully Hydrated Fluid Phase DMPC and DLPC Lipid Bilayers Using X-Ray Scattering From Oriented Multilamellar Arrays and From Unilamellar Vesicles Biophys. J. 2005, 88, 2626-2637
40. Blanton, T. N.; Huang, T. C.; Toraya, H.; Hubbard, C. R.; Robie, S. B.; Louër, D.; Göbel, H. E.; Will, G.; Gilles, R.; Raftery, T. JCPDS-International Centre for Diffraction Data Round Robin Study of Silver Behenate. A Possible Low-Angle X-Ray Diffraction Calibration Standard Powder Diffraction 1995, 10, 91-95
41. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. GROMACS: Fast, Flexible, and Free J. Comput. Chem. 2005, 26, 1701-1718
42. Klauda, J. B.; Venable, R. M.; Freites, J. A.; O'Connor, J. W.; Tobias, D. J.; Mondragon-Ramirez, C.; Vorobyov, I.; MacKerell, A. D., Jr.; Pastor, R. W. Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types J. Phys. Chem. B 2010, 114, 7830-7843
43. Abraham, M. J.; Van Der Spoel, D.; Lindahl, E.; Hess, B.; the GROMACS development team. GROMACS User Manual Version 5.0.2; www.gromacs.org, 2014.
44. Jo, S.; Kim, T.; Iyer, V. G.; Im, W. CHARMM-GUI: a Web-Based Graphical User Interface for CHARMM J. Comput. Chem. 2008, 29, 1859-1865
45. Bjelkmar, P.; Larsson, P.; Cuendet, M. A.; Hess, B.; Lindahl, E. Implementation of the CHARMM Force Field in GROMACS: Analysis of Protein Stability Effects From Correction Maps, Virtual Interaction Sites, and Water Models J. Chem. Theory Comput. 2010, 6, 459-466
46. Jämbeck, J. Downloads, Stockholm Lipids; http://people.su.se/~jjm/Stockholm-Lipids/Downloads.html, June 2013.
47. Piggot, T. J.; Pineiro, A.; Khalid, S. Molecular Dynamics Simulations of Phosphatidylcholine Membranes: A Comparative Force Field Study J. Chem. Theory Comput. 2012, 8, 4593-4609
48. Piggot, T. CHARMM36-Smaller Area Per Lipid for POPE-Why? http://permalink.gmane.org/gmane.science.biology.gromacs.user/53633, 2014.
49. Benz, R. W.; Castro-Roman, F.; Tobias, D. J.; White, S. H. Experimental Validation of Molecular Dynamics Simulations of Lipid Bilayers: a New Approach Biophys. J. 2005, 88, 805-817
50. Jensen, M. O.; Mouritsen, O. G.; Peters, G. H. Simulations of a Membrane-Anchored Peptide: Structure, Dynamics, and Influence on Bilayer Properties Biophys. J. 2004, 86, 3556-3575
51. Klauda, J. B.; Brooks, B. R.; MacKerell, A. D., Jr.; Venable, R. M.; Pastor, R. W. An Ab Initio Study on the Torsional Surface of Alkanes and Its Effect on Molecular Simulations of Alkanes and a DPPC Bilayer J. Phys. Chem. B 2005, 109, 5300-5311
52. Berger, O.; Edholm, O.; Jahnig, F. Molecular Dynamics Simulations of a Fluid Bilayer of Dipalmitoylphosphatidylcholine at Full Hydration, Constant Pressure, and Constant Temperature Biophys. J. 1997, 72, 2002-2013
53. Sapay, N.; Tieleman, D. P. Combination of the CHARMM27 Force Field With United-Atom Lipid Force Fields J. Comput. Chem. 2011, 32, 1400-1410
54. Feller, S. E.; Pastor, R. W. On Simulating Lipid Bilayers With an Applied Surface Tension: Periodic Boundary Conditions and Undulations Biophys. J. 1996, 71, 1350-1355
55. Feller, S. E.; Feller, S. E.; Zhang, Y.; Zhang, Y.; Pastor, R. W.; Pastor, R. W. Computer Simulation of Liquid/Liquid Interfaces. II. Surface Tension-Area Dependence of a Bilayer and Monolayer J. Chem. Phys. 1995, 103, 10267-10276
56. Jahnig, F. What Is the Surface Tension of a Lipid Bilayer Membrane? Biophys. J. 1996, 71, 1348-1349
57. Lindahl, E.; Edholm, O. Mesoscopic Undulations and Thickness Fluctuations in Lipid Bilayers From Molecular Dynamics Simulations Biophys. J. 2000, 79, 426-433
58. Marrink, S. J.; Mark, A. E. Effect of Undulations on Surface Tension in Simulated Bilayers J. Phys. Chem. B 2001, 105, 6122-6127
59. Marsh, D. Renormalization of the Tension and Area Expansion Modulus in Fluid Membranes Biophys. J. 1997, 73, 865-869
60. Skibinsky, A.; Venable, R. M.; Pastor, R. W. A Molecular Dynamics Study of the Response of Lipid Bilayers and Monolayers to Trehalose Biophys. J. 2005, 89, 4111-4121
61. Zhang, Y.; Zhang, Y.; Feller, S. E.; Feller, S. E.; Brooks, B. R.; Brooks, B. R.; Pastor, R. W.; Pastor, R. W. Computer Simulation of Liquid/Liquid Interfaces. I. Theory and Application to Octane/Water J. Chem. Phys. 1995, 103, 10252-10266
62. Klauda, J. B.; Kučerka, N.; Brooks, B. R.; Pastor, R. W.; Nagle, J. F. Simulation-Based Methods for Interpreting X-Ray Data From Lipid Bilayers Biophys. J. 2006, 90, 2796-2807
63. Anézo, C.; de Vries, A. H.; Holtje, H. D.; Tieleman, D. P.; Marrink, S. J. Methodological Issues in Lipid Bilayer Simulations J. Phys. Chem. B 2003, 107, 9424-9433
64. Sachs, J. N.; Petrache, H. I.; Woolf, T. B. Interpretation of Small Angle X-Ray Measurements Guided by Molecular Dynamics Simulations of Lipid Bilayers Chem. Phys. Lipids 2003, 126, 211-223
65. Klauda, J. B.; Monje, V.; Kim, T.; Im, W. Improving the CHARMM Force Field for Polyunsaturated Fatty Acid Chains J. Phys. Chem. B 2012, 116, 9424-9431
66. Kang, H.; Klauda, J. B. Molecular Dynamics Simulations of Palmitoyloleoylphosphatidylglycerol Bilayers Mol. Simul. 2014, 1-7
67. Kučerka, N.; Holland, B. W.; Gray, C. G.; Tomberli, B.; Katsaras, J. Scattering Density Profile Model of POPG Bilayers As Determined by Molecular Dynamics Simulations and Small-Angle Neutron and X-Ray Scattering Experiments J. Phys. Chem. B 2012, 116, 232-239
68. Pabst, G.; Rappolt, M.; Amenitsch, H.; Laggner, P. Structural Information From Multilamellar Liposomes at Full Hydration: Full Q-Range Fitting With High Quality X-Ray Data Phys. Rev. E 2000, 62, 4000-4009
69. 2H NMR Spectroscopy Biophys. J. 2000, 79, 3172-3192
70. McIntosh, T. J.; Simon, S. A. Area Per Molecule and Distribution of Water in Fully Hydrated Dilauroylphosphatidylethanolamine Bilayers Biochemistry 1986, 25, 4948-4952
71. Small, D. M. Phase Equilibria and Structure of Dry and Hydrated Egg Lecithin J. Lipid Res. 1967, 8, 551-557
72. Pink, D. A.; McNeil, S.; Quinn, B.; Zuckermann, M. J. A Model of Hydrogen Bond Formation in Phosphatidylethanolamine Bilayers Biochim. Biophys. Acta 1998, 1368, 289-305
73. Tristram-Nagle, S.; Zhang, R.; Suter, R. M.; Worthington, C. R.; Sun, W. J.; Nagle, J. F. Measurement of Chain Tilt Angle in Fully Hydrated Bilayers of Gel Phase Lecithins Biophys. J. 1993, 64, 1097-1109
74. Sun, W. J.; Tristram-Nagle, S.; Suter, R. M.; Nagle, J. F. Structure of Gel Phase Saturated Lecithin Bilayers: Temperature and Chain Length Dependence Biophys. J. 1996, 71, 885-891