Extracting Experimental Measurables from Molecular Dynamics Simulations of Membranes

Annual Reports in Computational Chemistry

Volumn 7, Issue , 2011, Pages 125-150

  Braun, Anthony R ^a   Sachs, Jonathan N ^a  

^a University of Minnesota   (United States)

Author keywords

Bilayer dynamics; Bilayer structure; Lipid bilayer; Molecular dynamics simulation; NMR relaxation rate; X ray scattering

Indexed keywords

EID: 80054043814     PISSN: 15741400     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-444-53835-2.00006-7     Document Type: Article

References (79)

1. van Gunsteren W.F., Dolenc J., Mark A.E. Molecular simulation as an aid to experimentalists. Curr. Opin. Struct. Biol. 2008, 18:149-153.
2. Nagle J.F., Tristram-Nagle S. Structure of lipid bilayers. Biochim. Biophys. Acta 2000, 1469:159-195.
3. Lewis B.A., Engelman D.M. Lipid bilayer thickness varies linearly with acyl chain-length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 1983, 166:211-217.
4. Lewis B.A., Engelman D.M. Bacteriorhodopsin remains dispersed in fluid phospholipid bilayers over a wide range of bilayer thicknesses. J. Mol. Biol. 1983, 166:203-210.
5. Cornea R.L., Thomas D.D. Efects of membrane thickness on the molecular dynamics and enzymatic activity of reconstituted CA-ATPase. Biochemistry 1994, 33:2912-2920.
6. Mitra K., Ubarretxena-Belandia I., Taguchi T., Warren G., Engelman D.M. Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:4083-4088.
7. Hatzakis N.S., Bhatia V.K., Larsen J., Madsen K.L., Bolinger P.-Y., Kunding A.H., Castillo J., Gether U., Hedegard P., Stamou D. How curved membranes recruit amphipathic helices and protein anchoring motifs. Nat. Chem. Biol. 2009, 5:835-841.
8. Killian J.A., von Heijne G. How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 2000, 25:429-434.
9. Weiss T., van der Wel P., Killian J., Koeppe R., Huang H. Hydrophobic mismatch between helices and lipid bilayers. Biophys. J. 2003, 84:379-385.
10. Benz R.W., Castro-Román 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.
11. 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.
12. Kuerka N., Perlmutter J.D., Pan J., Tristram-Nagle S., Katsaras J., Sachs J.N. The efect of cholesterol on short- and long-chain monounsaturated lipid bilayers as determined by molecular dynamics simulations and X-ray scattering. Biophys. J. 2008, 95:2792-2805.
13. Braun A.R., Brandt E.G., Edholm O., Nagle J.F., Sachs J.N. Determination of electron density profiles and area from simulations of undulating membranes. Biophys. J. 2011, 100:2112-2120.
14. Petrache H., Tristram-Nagle S., Harries D., Kucerka N., Nagle J., Parsegian V. Swelling of phospholipids by monovalent salt. J. Lipid Res. 2006, 47:302-309.
15. Kucerka 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.
16. Kuerka 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.
17. Petrache H., Tristram-Nagle S., Nagle J. Fluid phase structure of EPC and DMPC bilayers. Chem. Phys. Lipids 1998, 95:83-94.
18. McIntosh T.J., Simon S.A. Area per molecule and distribution of water in fully hydrated dilauroylphosphatidylethanolamine. Biochemistry 1986, 25:4948-4952.
19. Ludtke S., He K., Huang H. Membrane thinning caused by magainin 2. Biochemistry 1995, 34:16764-16769.
20. Wiener M., White S. Fluid bilayer structure determination by the combined use of X-ray and neutron diffraction. I. Fluid bilayer models and the limits of resolution. Biophys. J. 1991, 59:162-173.
21. Janiak M.J., Small D.M., Shipley G.G. Temperature and compositional dependence of the structure of hydrated dimyristoyl lecithin. J. Biol. Chem. 1979, 254:6068-6078.
22. Wilkins M.H.F., Blaurock A.E., Engelman D.M. Bilayer structure in membranes. Nat. New Biol. 1971, 230:72-76.
23. Schalke M., Kruger P., Weygand M., Losche M. Submolecular organization of DMPA in surface monolayers: Beyond the two-layer model. Biochim. Biophys. Acta 2000, 1464:113-126.
24. Wiener M., Suter R., Nagle J. Structure of the fully hydrated gel phase of dipalmitoylphosphatidylcholine. Biophys. J. 1989, 55:315-325.
25. Klauda J.B., Kuerka 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.
26. Kurka N., Katsaras J., Nagle J.F. Comparing membrane simulations to scattering experiments: Introducing the SIMtoEXP software. J. Membr. Biol. 2010, 235:43-50.
27. Feller S.E., Venable R.M., Pastor R.W. Computer simulation of a DPPC phospholipid bilayer: Structural changes as a function of molecular surface area. Langmuir 1997, 13:6555-6561.
28. Cromer D.T., Mann J.B. X-ray scattering factors computed from numerical Hartree-Fock wave functions. Acta Crystallogr. A 1968, 24:321-324.
29. Brandt E.G., Braun A.R., Sachs J.N., Nagle J.F., Edholm O. Interpretation of fluctuation spectra in simulations of lipid bilayers. Biophys. J. 2010, 100:2104-2111.
30. Veatch S.L., Keller S.L. A closer look at the canonical "raft mixture" in model membrane studies. Biophys. J. 2003, 84:725-726.
31. Feigenson G.W. Phase diagrams and lipid domains in multicomponent lipid bilayer mixtures. Biochim. Biophys. Acta 2009, 1788:47-52.
32. Veatch S., Polozov I., Gawrisch K., Keller S. Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys. J. 2004, 86:2910-2922.
33. Veatch S.L., Soubias O., Keller S.L., Gawrisch K. Critical fluctuations in domain-forming lipid mixtures. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:17650-17655.
34. Veatch S.L., Cicuta P., Sengupta P., Honerkamp-Smith A., Holowka D., Baird B. Critical fluctuations in plasma membrane vesicles. ACS Chem. Biol. 2008, 3:287-293.
35. Veatch S.L., Leung S.S.W., Hancock R.E.W., Thewalt J.L. Fluorescent probes alter miscibility phase boundaries in ternary vesicles. J. Phys. Chem. B 2007, 111:502-504.
36. Feigenson G.W. Phase boundaries and biological membranes. Annu. Rev. Biophys. Biomol. Struct. 2007, 36:63-77.
37. Salditt T. Structure and fluctuations of highly oriented phospholipid membranes. Curr. Opin. Colloid Interface Sci. 2000, 5:19-26.
38. Spaar A., Salditt T. Short range order of hydrocarbon chains in fluid phospholipid bilayers studied by X-ray difraction from highly oriented membranes. Biophys. J. 2003, 85:1576-1584.
39. Mills T.T., Toombes G.E., Tristram-Nagle S., Smilgies D.-M., Feigenson G.W., Nagle J.F. Order parameters and areas in fluid-phase oriented lipid membranes using wide angle X-ray scattering. Biophys. J. 2008, 95:669-681.
40. Mills T.T., Tristram-Nagle S., Heberle F.A., Morales N.F., Zhao J., Wu J., Toombes G.E.S., Nagle J.F., Feigenson G.W. Liquid-liquid domains in bilayers detected by wide angle X-ray scattering. Biophys. J. 2008, 95:682-690.
41. Mills T.T., Huang J., Feigenson G.W., Nagle J.F. Efects of cholesterol and unsaturated DOPC lipid on chain packing of saturated gel-phase DPPC bilayers. Gen. Physiol. Biophys. 2009, 28:126-139.
42. Sega M., Garberoglio G., Brocca P., Cantü L. Reconstruction of atomistic details from coarse-grained structures. J. Phys. Chem. B 2007, 111:2484-2489.
43. Hub J.S., Salditt T., Rheinstädter M.C., de Groot B.L. Short-range order and collective dynamics of DMPC bilayers: A comparison between molecular dynamics simulations, X-ray, and neutron scattering experiments. Biophys. J. 2007, 93:3156-3168.
44. Brown M.F., Ribeiro A.A., Williams G.D. New view of lipid bilayer dynamics from H-2 and C-13 NMR relaxation-time measurements. Proc. Natl. Acad. Sci. U.S.A. 1983, 80:4325-4329.
45. Brown M., Thurmond R., Dodd S., Otten D., Beyer K. Composite membrane deformation on the mesoscopic length scale. Phys. Rev. E 2001, 64:010901.
46. Brown M., Thurmond R., Dodd S., Otten D., Beyer K. Elastic deformation of membrane bilayers probed by deuterium NMR relaxation. J. Am. Chem. Soc. 2002, 124:8471-8484.
47. Brown M.F. Theory of spin-lattice relaxation in lipid bilayers and biological membranes-Dipolar relaxation. J. Chem. Phys. 1984, 80:2808-2831.
48. Leftin A., Brown M.F. An NMR database for simulations of membrane dynamics. Biochim. Biophys. Acta 2011, 1808:818-839.
49. Pastor R.W., Venable R.M., Karplus M. Brownian dynamics simulation of a lipid chain in a membrane bilayer. J. Chem. Phys. 1988, 89:1112-1127.
50. Pastor R.W., Venable R.M., Karplus M., Scabo A. A simulation based model of NMR T1 relaxation in lipid bilayer vesicles. J. Chem. Phys. 1988, 89:1128-1140.
51. Klauda J.B., Roberts M.F., Redfield A.G., Brooks B.R., Pastor R.W. Rotation of lipids in membranes: Molecular dynamics simulation, 31P spin-lattice relaxation, and rigid-body dynamics. Biophys. J. 2008, 89:1128-1140.
52. Pastor R.W., Venable R.M., Feller S.E. Lipid bilayers, NMR relaxation, and computer simulations. Acc. Chem. Res. 2002, 35:438-446.
53. Feller S.E., Huster D., Gawrisch K. Interpretation of NOESY cross-relaxation rates from molecular dynamics simulation of a lipid bilayer. J. Am. Chem. Soc. 1999, 121:8963-8964.
54. Lindahl E., Edholm O. Molecular dynamics simulation of NMR relaxation rates and slow dynamics in lipid bilayers. J. Chem. Phys. 2001, 115:4938-4950.
55. Wohlert J., Edholm O. Dynamics in atomistic simulations of phospholipid membranes: Nuclear magnetic resonance relaxation rates and lateral difusion. J. Chem. Phys. 2006, 125:204703.
56. Klauda J.B., Eldho N.V., Gawrisch K., Brooks B.R., Pastor R.W. Collective and noncollective models of NMR relaxation in lipid vesicles and multilayers. J. Phys. Chem. B 2008, 112:5924-5929.
57. Klauda J.B., Venable R.M., Freites J.A., O'Connor J.W., Tobias D.J., Mondragon-Ramirez C., Vorobyov I., MacKerell A.D., 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.
58. Berger O., Edholm O., Jähnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 1997, 72:2002-2013.
59. Chiu S.-W., Pandit S.A., Scott H.L., Jakobsson E. An improved united atom force field for simulation of mixed lipid bilayers. J. Phys. Chem. B 2009, 113:2748-2763.
60. Roberts M.F., Redfield A.G. High-resolution P-31 field cycling NMR as a probe of phospholipid dynamics. J. Am. Chem. Soc. 2004, 126:13765-13777.
61. Marrink S.J., Risselada H.J., Yefimov S., Tieleman D.P., de Vries A.H. The MARTINI force field: Coarse grained model for biomolecular simulations. J. Phys. Chem. B 2007, 111:7812-7824.
62. Sansom M.S.P., Scott K.A., Bond P.J. Coarse-grained simulation: A high-throughput computational approach to membrane proteins. Biochem. Soc. Trans. 2008, 36:27-32.
63. Ayton G.S., Lyman E., Voth G.A. Hierarchical coarse-graining strategy for protein-membrane systems to access mesoscopic scales. Faraday Discuss. 2010, 144:347-357.
64. Hills R.D., Lu L., Voth G.A. Multiscale coarse-graining of the protein energy landscape. PLoS Comput. Biol. 2010, 6:e1000827.
65. Tumaneng P.W., Pandit S.A., Zhao G., Scott H.L. Lateral organization of complex lipid mixtures from multiscale modeling. J. Chem. Phys. 2010, 132:065104.
66. Baoukina S., Tieleman D.P. Direct simulation of protein-mediated vesicle fusion: Lung surfactant protein B. Biophys. J. 2010, 99:2134-2142.
67. Louhivuori M., Risselada H.J., van der Giessen E., Marrink S.J. Release of content through mechano-sensitive gates in pressurized liposomes. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:19856-19860.
68. Perlmutter J.D., Sachs J.N. Experimental verification of lipid bilayer structure through multi-scale modeling. Biochim. Biophys. Acta 2009, 1788:2284-2290.
69. Shih A.Y., Freddolino P.L., Sligar S.G., Schulten K. Disassembly of nanodiscs with cholate. Nano Lett. 2007, 7:1692-1696.
70. Rzepiela A.J., Schäfer L.V., Goga N.H., Risselada J., De Vries A.H., Siewert J.M. Reconstruction of atomistic details from coarse-grained structures. J. Comput. Chem. 2010, 31:1333-1343.
71. Ali M.R., Cheng K.H., Huang J. Assess the nature of cholesterol-lipid interactions through the chemical potential of cholesterol in phosphatidylcholine bilayers. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5372-5377.
72. Coppock P.S., Kindt J.T. Atomistic simulations of mixed-lipid bilayers in gel and fluid phases. Langmuir 2009, 25:352-359.
73. Kokubo H., Okamoto Y. Prediction of membrane protein structures by replica-exchange Monte Carlo simulations: Case of two helices. J. Chem. Phys. 2004, 120:10837-10847.
74. Im W., Brooks C. Interfacial folding and membrane insertion of designed peptides studied by molecular dynamics simulations. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:6771-6776.
75. Nymeyer H., Woolf T., Garcia A. Folding is not required for bilayer insertion: Replica exchange simulations of an alpha-helical peptide with an explicit lipid bilayer. Proteins 2005, 59:783-790.
76. Roux B., Allen T., Berneche S., Im W. Theoretical and computational models of biological ion channels. Q. Rev. Biophys. 2004, 37:15-103.
77. MacCallum J.L., Bennett W.F.D., Tieleman D.P. Distribution of amino acids in a lipid bilayer from computer simulations. Biophys. J. 2008, 94:3393-3404.
78. Bennett W.F.D., MacCallum J.L., Tieleman D.P. Thermodynamic analysis of the efect of cholesterol on dipalmitoylphosphatidylcholine lipid membranes. J. Am. Chem. Soc. 2009, 131:1972-1978.
79. Grossfield, A., 2010. WHAM: The weighted histogram analysis method. http://www.membrane.urmc.rochester.edu/content/wham.