A microscopic view of phospholipid insertion into biological membranes

Journal of Physical Chemistry B

Volumn 118, Issue 7, 2014, Pages 1754-1764

  Vermaas, Josh V ^a   Tajkhorshid, Emad ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CYTOLOGY; MEMBRANES;

COMPARATIVE STUDIES; MECHANISTIC MODELING; MEMBRANE ASSOCIATION; MEMBRANE INTERFACE; PERIPHERAL MEMBRANES; PHOSPHOLIPID BILAYER; RATE-LIMITING STEPS; SEQUENTIAL INSERTION;

PHOSPHOLIPIDS;

1,1 DICHLOROETHANE; 1,1-DICHLOROETHANE; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; BIOMIMETIC MATERIAL; CHLOROETHANE; DRUG DERIVATIVE; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID;

ARTICLE; ARTIFICIAL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; LIPID BILAYER; MOLECULAR DYNAMICS; PROBABILITY; STATISTICAL MODEL; TIME;

BIOMIMETIC MATERIALS; ETHYL CHLORIDE; LINEAR MODELS; LIPID BILAYERS; MEMBRANES, ARTIFICIAL; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLCHOLINES; PHOSPHOLIPIDS; PROBABILITY; TIME FACTORS;

EID: 84894099024     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp409854w     Document Type: Article

References (67)

1. Liu, L.-N.; Bryan, S. J.; Huang, F.; Yu, J.; Nixon, P. J.; Rich, P. R.; Mullineaux, C. W. Control of Electron Transport Routes Through Redox-Regulated Redistribution of Respiratory Complexes Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 11431-11436
2. Foyer, C. H.; Neukermans, J.; Queval, G.; Noctor, G.; Harbinson, J. Photosynthetic Control of Electron Transport and the Regulation of Gene Expression J. Exp. Bot. 2012, 63, 1637-1661
3. Sadiq, S.; Guixa-Gonzalez, R.; Dainese, E.; Pastor, M.; De Fabritiis, G.; Selent, J. Molecular Modeling and Simulation of Membrane Lipid-Mediated Effects on GPCRs Curr. Med. Chem. 2013, 20, 22-38
4. Grafmüller, A.; Lipowsky, R.; Knecht, V. Effect of Tension and Curvature on the Chemical Potential of Lipids in Lipid Aggregates Phys. Chem. Chem. Phys. 2013, 15, 876-881
5. Grafmüller, A.; Shillcock, J.; Lipowsky, R. The Fusion of Membranes and Vesicles: Pathway and Energy Barriers from Dissipative Particle Dynamics Biophys. J. 2009, 96, 2658-2675
6. Nagle, J. F.; Tristram-Nagle, S. Structure of Lipid Bilayers Biochim. Biophys. Acta 2000, 1469, 159-195
7. Phillips, R.; Ursell, T.; Wiggins, P.; Sens, P. Emerging Roles for Lipids in Shaping Membrane-Protein Function Nature 2009, 459, 379-384
8. Lev, S. Non-Vesicular Lipid Transport by Lipid-Transfer Proteins and Beyond Nat. Rev. Mol. Cell Biol. 2010, 11, 739-750
9. Barbacci, D.; Jackson, S. N.; Muller, L.; Egan, T.; Lewis, E. K.; Schultz, J. A.; Woods, A. S. Cellular Membrane Phospholipids Act As a Depository for Quaternary Amine Containing Drugs Thus Competing with the Acetylcholine/Nicotinic Receptor J. Proteome Res. 2012, 11, 3382-3389
10. Romsicki, Y.; Sharom, F. J. the Membrane Lipid Environment Modulates Drug Interactions with the P-Glycoprotein Multidrug Transporter Biochemistry 1999, 38, 6887-6896
11. R. Neves, A.; Lucio, M.; L.C. Lima, J.; Reis, S. Resveratrol in Medicinal Chemistry: A Critical Review of Its Pharmacokinetics, Drug-Delivery, and Membrane Interactions Curr. Med. Chem. 2012, 19, 1663-1681
12. Kopeć, W.; Telenius, J.; Khandelia, H. Molecular Dynamics Simulations of the Interactions of Medicinal Plant Extracts and Drugs with Lipid Bilayer Membranes FEBS J. 2013, 280, 2785-2805
13. Cerasoli, E.; Ravi, J.; Gregor, C.; Hussain, R.; Siligardi, G.; Martyna, G.; Crain, J.; Ryadnov, M. G. Membrane Mediated Regulation in Free Peptides of HIV-1 Gp41: Minimal Modulation of the Hemifusion Phase Phys. Chem. Chem. Phys. 2012, 14, 1277-1285
14. Sun, X.; Shi, J.; Delaloye, K.; Yang, X.; Yang, H.; Zhang, G.; Cui, J. the Interface Between Membrane-Spanning and Cytosolic Domains in Ca2+-Dependent K+ Channels Is Involved in β Subunit Modulation of Gating J. Neurosci. 2013, 33, 11253-11261
15. Ahn, T.; Yun, C.-H.; Kim, H.-R.; Chae, H.-J. Cardiolipin, Phosphatidylserine, and BH4 Domain of Bcl-2 Family Regulate Ca2+/H+ Antiporter Activity of Human Bax Inhibitor-1 Cell Calcium 2010, 47, 387-396
16. 2+, Phosphatidylserine and Diacylglycerol Required for Protein Kinase C α to Reach Maximum Activity PLoS One 2013, 8, e69041
17. Vogel, A.; Reuther, G.; Roark, M. B.; Tan, K.-T.; Waldmann, H.; Feller, S. E.; Huster, D. Backbone Conformational Flexibility of the Lipid Modified Membrane Anchor of the Human N-Ras Protein Investigated by Solid-State NMR and Molecular Dynamics Simulation Biochim. Biophys. Acta, Biomembr. 2010, 1798, 275-285
18. Vogel, A.; Roark, M.; Feller, S. E. A Reinterpretation of Neutron Scattering Experiments on a Lipdated Ras Peptide Using Replica Exchange Molecular Dynamics Biochim. Biophys. Acta, Biomembr. 2012, 1818, 219-224
19. Markwick, P. R. L.; Pierce, L. C. T.; Goodin, D. B.; McCammon, J. A. Adaptive Accelerated Molecular Dynamics (Ad-AMD) Revealing the Molecular Plasticity of P450cam J. Phys. Chem. Lett. 2011, 2, 158-164
20. Smirnova, Y. G.; Marrink, S.-J.; Lipowsky, R.; Knecht, V. Solvent-Exposed Tails As Prestalk Transition States for Membrane Fusion at Low Hydration J. Am. Chem. Soc. 2010, 132, 6710-6718
21. Chill, J. H.; Naider, F. A Solution NMR View of Protein Dynamics in the Biological Membrane Curr. Opin. Struct. Biol. 2011, 21, 627-633
22. Holzer, R. G.; Park, E.-J.; Li, N.; Tran, H.; Chen, M.; Choi, C.; Solinas, G.; Karin, M. Saturated Fatty Acids Induce C-Src Clustering Within Membrane Subdomains, Leading to JNK Activation Cell 2011, 147, 173-184
23. Antonny, B. Mechanisms of Membrane Curvature Sensing Annu. Rev. Biochem. 2011, 80, 101-123
24. Kusumi, A.; Nakada, C.; Ritchie, K.; Murase, K.; Suzuki, K.; Murakoshi, H.; Kasai, R. S.; Kondo, J.; Fujiwara, T. Paradigm Shift of the Plasma Membrane Concept from the Two-Dimensional Continuum Fluid to the Partitioned Fluid: High-Speed Single-Molecule Tracking of Membrane Molecules Annu. Rev. Biophys. Biomol. Struct. 2005, 34, 351-378
25. Morrissey, J. H.; Tajkhorshid, E.; Rienstra, C. M. Nanoscale Studies of Protein-Membrane Interactions in Blood Clotting J. Thromb. Haemostasis 2011, 9 (Suppl. 1) 167-167
26. Wen, P.-C.; Huang, Z.; Enkavi, G.; Wang, Y.; Gumbart, J.; Tajkhorshid, E. Molecular Mechanisms of Active Transport Across the Cellular Membrane. In Molecular Simulations and Biomembranes: From Biophysics to Function; Biggin, P.; Sansom, M., Eds.; Royal Society of Chemistry: London, 2010; pp 248-286.
27. Shaikh, S. A.; Wen, P.-C.; Enkavi, G.; Huang, Z.; Tajkhorshid, E. Capturing Functional Motions of Membrane Channels and Transporters with Molecular Dynamics Simulation J. Comput. Theor. Nanosci. 2010, 7, 2481-2500
28. Shimamura, T.; Weyand, S.; Beckstein, O.; Rutherford, N. G.; Hadden, J. M.; Sharples, D.; Sansom, M. S. P.; Iwata, S.; Henderson, P. J. F.; Cameron, A. D. Molecular Basis of Alternating Access Membrane Transport by the Sodium-Hydantoin Transporter Mhp1 Science 2010, 328, 470-473
29. Nury, H.; Poitevin, F.; Van Renterghem, C.; Changeux, J.-P.; Corringer, P.-J.; Delarue, M.; Baaden, M. One-Microsecond Molecular Dynamics Simulation of Channel Gating in a Nicotinic Receptor Homologue Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 6275-6280
30. Kruse, A. C.; Hu, J.; Pan, A. C.; Arlow, D. H.; Rosenbaum, D. M.; Rosemond, E.; Green, H. F.; Liu, T.; Chae, P. S.; Dror, R. O. Structure and Dynamics of the M3Muscarinic Acetylcholine Receptor Nature 2012, 482, 552-556
31. 2+ in Membrane Binding of Blood Coagulation Factors Structure 2008, 16, 72-81
32. Arcario, M. J.; Ohkubo, Y. Z.; Tajkhorshid, E. Capturing Spontaneous Partitioning of Peripheral Proteins Using a Biphasic Membrane-Mimetic Model J. Phys. Chem. B 2011, 115, 7029-7037
33. den Otter, W. K.; Shkulipa, S. A. Intermonolayer Friction and Surface Shear Viscosity of Lipid Bilayer Membranes Biophys. J. 2007, 93, 423-433
34. 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
35. Im, W.; Feig, M.; Brooks, C. L., III An Implicit Membrane Generalized Born Theory for the Study of Structure, Stability, and Interactions of Membrane Proteins Biophys. J. 2003, 85, 2900-2918
36. Panahi, A.; Feig, M. Dynamic Heterogeneous Dielectric Generalized Born (DHDGB): An Implicit Membrane Model with a Dynamically Varying Bilayer Thickness J. Chem. Theor. Comput. 2013, 9, 1709-1719
37. Lazaridis, T. Effective Energy Function for Proteins in Lipid Membranes Proteins 2003, 52, 176-192
38. Ulmschneider, M. B.; Sansom, M. S. P.; Di Nola, A. Properties of Integral Membrane Protein Structures: Derivation of an Implicit Membrane Potential Proteins 2005, 59, 252-265
39. Ohkubo, Y. Z.; Pogorelov, T. V.; Arcario, M. J.; Christensen, G. A.; Tajkhorshid, E. Accelerating Membrane Insertion of Peripheral Proteins with a Novel Membrane Mimetic Model Biophys. J. 2012, 102, 2130-2139
40. Hamelberg, D.; Mongan, J.; McCammon, J. A. Accelerated Molecular Dynamics: A Promising and Efficient Simulation Method for Biomolecules J. Chem. Phys. 2004, 120, 11919-11929
41. Pierce, L. C.; Salomon-Ferrer, R.; Augusto, F.; de Oliveira, C.; McCammon, J. A.; Walker, R. C. Routine Access to Millisecond Time Scale Events with Accelerated Molecular Dynamics J. Chem. Theory Comput. 2012, 8, 2997-3002
42. Martin, F. J.; MacDonald, R. C. Phospholipid Exchange Between Bilayer Membrane Vesicles Biochemistry 1976, 15, 321-327
43. McLean, L. R.; Phillips, M. C. Mechanism of Cholesterol and Phosphatidylcholine Exchange or Transfer Between Unilamellar Vesicles Biochemistry 1981, 20, 2893-2900
44. Roseman, M. A.; Thompson, T. E. Mechanism of the Spontaneous Transfer of Phospholipids Between Bilayers Biochemistry 1980, 19, 439-444
45. Jones, J. D.; Thompson, T. E. Mechanism of Spontaneous, Concentration-Dependent Phospholipid Transfer Between Bilayers Biochemistry 1990, 29, 1593-1600
46. Lev, S. Nonvesicular Lipid Transfer from the Endoplasmic Reticulum Cold Spring Harbor Perspect. Biol. 2012, 4, a013300
47. Nichols, J. W.; Pagano, R. E. Kinetics of Soluble Lipid Monomer Diffusion Between Vesicles Biochemistry 1981, 20, 2783-2789
48. Tieleman, D. P.; Marrink, S.-J. Lipids out of Equilibrium: Energetics of Desorption and Pore Mediated Flip-Flop J. Am. Chem. Soc. 2006, 128, 12462-12467
49. Kučerka, N.; Tristram-Nagle, S.; Nagle, J. F. Structure of Fully Hydrated Fluid Phase Lipid Bilayers with Monounsaturated Chains J. Membr. Biol. 2005, 208, 193-202
50. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38
51. 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
52. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
53. 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
54. Darden, T.; York, D.; Pedersen, L. G. Particle Mesh Ewald: An N ·log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
55. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A Smooth Particle Mesh Ewald Method J. Chem. Phys. 1995, 103, 8577-8593
56. Martyna, G. J.; Tobias, D. J.; Klein, M. L. Constant Pressure Molecular Dynamics Algorithms J. Chem. Phys. 1994, 101, 4177-4189
57. Feller, S. E.; Zhang, Y.; Pastor, R. W.; Brooks, B. R. Constant Pressure Molecular Dynamics Simulation: The Langevin Piston Method J. Chem. Phys. 1995, 103, 4613-4621
58. Nobile, A. G.; Ricciardi, L. M.; Sacerdote, L. Exponential Trends of Ornstein-Uhlenback First-Passage-Time Densities J. Appl. Probab. 1985, 22, 360-369
59. Swope, W. C.; Pitera, J. W.; Suits, F. Describing Protein Folding Kinetics by Molecular Dynamics Simulations. 1. Theory J. Phys. Chem. B 2004, 108, 6571-6581
60. Voelz, V. A.; Bowman, G. R.; Beauchamp, K.; Pande, V. S. Molecular Simulation of Ab Initio Protein Folding for a Millisecond Folder NTL9(1-39) J. Am. Chem. Soc. 2010, 132, 1526-1528
61. Elmer, S. P.; Park, S.; Pande, V. S. Foldamer Dynamics Expressed Via Markov State Models. I. Explicit Solvent Molecular-Dynamics Simulations in Acetonitrile, Chloroform, Methanol and Water J. Chem. Phys. 2005, 123, 114902
62. Chodera, J. D.; Singhal, N.; Pande, V. S.; Dill, K. A.; Swope, W. C. Automatic Discovery of Metastable States for the Construction of Markov Models of Macromolecular Conformational Dynamics J. Chem. Phys. 2007, 126, 155101
63. Berg, B. A.; Harris, R. C. From Data to Probability Densities Without Histograms Comput. Phys. Commun. 2008, 179, 443-448
64. Heller, H.; Schaefer, M.; Schulten, K. Molecular Dynamics Simulation of a Bilayer of 200 Lipids in the Gel and in the Liquid Crystal-Phases J. Phys. Chem. 1993, 97, 8343-8360
65. +-Lipid Interactions and Finite Size Effects Biophys. J. 2008, 94, 3565-3576
66. Castro-Román, F.; Benz, R. W.; White, S. H.; Tobias, D. J. Investigation of Finite System-Size Effects in Molecular Dynamics Simulations of Lipid Bilayers J. Phys. Chem. B 2006, 110, 24157-24164
67. Yeh, I.-C.; Hummer, G. System-Size Dependence of Diffusion Coefficients and Viscosities from Molecular Dynamics Simulations with Periodic Boundary Conditions J. Phys. Chem. B 2004, 108, 15873-15879