Toward Atomistic Resolution Structure of Phosphatidylcholine Headgroup and Glycerol Backbone at Different Ambient Conditions

Journal of Physical Chemistry B

Volumn 119, Issue 49, 2015, Pages 15075-15088

  Botan, Alexandru ^a   Favela Rosales, Fernando ^b   Fuchs, Patrick F J ^c   Javanainen, Matti ^d   Kanduč, Matej ^e   Kulig, Waldemar ^d   Lamberg, Antti ^f   Loison, Claire ^a   Lyubartsev, Alexander ^g   Miettinen, Markus S ^e   Monticelli, Luca ^h   Määttä, Jukka ⁱ   Ollila, O H Samuli ⁱ   Retegan, Marius ^j   Róg, Tomasz ^d   Santuz, Hubert ^k,l,m,n   Tynkkynen, Joona ^d  

^a UNIVERSITÉ LYON 1   (France)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c INSTITUT JACQUES MONOD   (France)

^d TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

^f KYOTO UNIVERSITY   (Japan)

^g STOCKHOLM UNIVERSITY   (Sweden)

^h INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

ⁱ AALTO UNIVERSITY   (Finland)

^j MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^k INSERM   (France)

^l UNIVERSITÉ PARIS DESCARTES   (France)

^m INSTITUT NATIONAL DE LA TRANSFUSION SANGUINE   (France)

ⁿ Laboratory of Excellence GR Ex   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CHOLESTEROL; CYTOLOGY; GLYCEROL; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPIDS;

ATOMISTIC RESOLUTION; CHEMICAL INFORMATION; COMMUNICATION PLATFORMS; DIMENSIONAL REPRESENTATION; INTERPRETATION TOOLS; MOLECULAR DYNAMICS SIMULATIONS; PHOSPHATIDYLCHOLINE; SCIENTIFIC CONTRIBUTIONS;

LIPID BILAYERS;

GLYCEROL; PHOSPHATIDYLCHOLINE;

CARBON NUCLEAR MAGNETIC RESONANCE; CHEMICAL STRUCTURE; CHEMISTRY; PROTON NUCLEAR MAGNETIC RESONANCE;

CARBON-13 MAGNETIC RESONANCE SPECTROSCOPY; GLYCEROL; MOLECULAR STRUCTURE; PHOSPHATIDYLCHOLINES; PROTON MAGNETIC RESONANCE SPECTROSCOPY;

EID: 84949575664     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b04878     Document Type: Article

References (159)

1. Structure and Dynamics of Membranes; Lipowsky, R., Sackmann, E., Eds.; Elsevier: New York, 1995.
2. Tieleman, D. P.; Marrink, S. J.; Berendsen, H. J. C. A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems Biochim. Biophys. Acta, Rev. Biomembr. 1997, 1331, 235-270 10.1016/S0304-4157(97)00008-7
3. Klauda, J. B.; Venable, R. M.; MacKerell, A. D., Jr.; Pastor, R. W. In Computational Modeling of Membrane Bilayers; Feller, S. E., Ed.; Current Topics in Membranes; Academic Press: New York, 2008; Vol. 60; pp 1-48.
4. Edholm, O. In Computational Modeling of Membrane Bilayers; Feller, S. E., Ed.; Current Topics in Membranes; Academic Press: New York, 2008; Vol. 60; pp 91-110.
5. Tieleman, D. P. In Molecular Simulations and Biomembranes: From Biophysics to Function; Sansom, M.; Biggin, P., Eds.; The Royal Society of Chemistry: London, 2010; pp 1-25.
6. Piggot, T. J.; Piñeiro, á; Khalid, S. Molecular Dynamics Simulations of Phosphatidylcholine Membranes: A Comparative Force Field Study J. Chem. Theory Comput. 2012, 8, 4593-4609 10.1021/ct3003157
7. Rabinovich, A.; Lyubartsev, A. Computer simulation of lipid membranes: Methodology and achievements Polym. Sci., Ser. C 2013, 55, 162-180 10.1134/S1811238213070060
8. Marsh, D. Handbook of Lipid Bilayers, 2nd ed.; RSC Press: London, 2013.
9. Israelachvili, J. N.; Marcelja, S.; Horn, R. G. Physical Principles of Membrane Organization Q. Rev. Biophys. 1980, 13, 121-200 10.1017/S0033583500001645
10. Seelig, J.; Gally, H.-U.; Wohlgemuth, R. Orientation and flexibility of the choline head group in phosphatidylcholine bilayers Biochim. Biophys. Acta, Biomembr. 1977, 467, 109-119 10.1016/0005-2736(77)90188-2
11. Skarjune, R.; Oldfield, E. Physical studies of cell surface and cell membrane structure. Determination of phospholipid head group organization by deuterium and phosphorus nuclear magnetic resonance spectroscopy Biochemistry 1979, 18, 5903-5909 10.1021/bi00593a022
12. Jacobs, R. E.; Oldfield, E. NMR of membranes Prog. Nucl. Magn. Reson. Spectrosc. 1980, 14, 113-136 10.1016/0079-6565(80)80006-9
13. Davis, J. H. The description of membrane lipid conformation, order and dynamics by 2H-NMR Biochim. Biophys. Acta, Rev. Biomembr. 1983, 737, 117-171 10.1016/0304-4157(83)90015-1
14. Strenk, L.; Westerman, P.; Doane, J. A model of orientational ordering in phosphatidylcholine bilayers based on conformational analysis of the glycerol backbone region Biophys. J. 1985, 48, 765-773 10.1016/S0006-3495(85)83834-0
15. Akutsu, H.; Nagamori, T. Conformational analysis of the polar head group in phosphatidylcholine bilayers: a structural change induced by cations Biochemistry 1991, 30, 4510-4516 10.1021/bi00232a020
16. Hong, M.; Schmidt-Rohr, K.; Nanz, D. Study of phospholipid structure by 1H, 13C, and 31P dipolar couplings from two-dimensional NMR Biophys. J. 1995, 69, 1939-1950 10.1016/S0006-3495(95)80064-0
17. Hong, M.; Schmidt-Rohr, K.; Zimmermann, H. Conformational Constraints on the Headgroup and sn-2 Chain of Bilayer DMPC from NMR Dipolar Couplings Biochemistry 1996, 35, 8335-8341 10.1021/bi953083i
18. Semchyschyn, D. J.; Macdonald, P. M. Conformational response of the phosphatidylcholine headgroup to bilayer surface charge: torsion angle constraints from dipolar and quadrupolar couplings in bicelles Magn. Reson. Chem. 2004, 42, 89-104 10.1002/mrc.1333
19. Hauser, H.; Guyer, W.; Pascher, I.; Skrabal, P.; Sundell, S. Polar group conformation of phosphatidylcholine. Effect of solvent and aggregation Biochemistry 1980, 19, 366-373 10.1021/bi00543a018
20. Hauser, H.; Guyer, W.; Paltauf, F. Polar group conformation of 1,2-di-O-alkylglycerophosphocholines in the absence and presence of ions Chem. Phys. Lipids 1981, 29, 103-120 10.1016/0009-3084(81)90076-1
21. Hauser, H.; Pascher, I.; Pearson, R.; Sundell, S. Preferred conformation and molecular packing of phosphatidylethanolamine and phosphatidylcholine Biochim. Biophys. Acta, Rev. Biomembr. 1981, 650, 21-51 10.1016/0304-4157(81)90007-1
22. Akutsu, H. Direct determination by Raman scattering of the conformation of the choline group in phospholipid bilayers Biochemistry 1981, 20, 7359-7366 10.1021/bi00529a006
23. Pascher, I.; Lundmark, M.; Nyholm, P.-G.; Sundell, S. Crystal structures of membrane lipids Biochim. Biophys. Acta, Rev. Biomembr. 1992, 1113, 339-373 10.1016/0304-4157(92)90006-V
24. Hauser, H.; Pascher, I.; Sundell, S. Preferred conformation and dynamics of the glycerol backbone in phospholipids. An NMR and x-ray single-crystal analysis Biochemistry 1988, 27, 9166-9174 10.1021/bi00426a014
25. Marsh, D.; Páli, T. Lipid conformation in crystalline bilayers and in crystals of transmembrane proteins Chem. Phys. Lipids 2006, 141, 48-65 10.1016/j.chemphyslip.2006.02.005
26. Gally, H. U.; Pluschke, G.; Overath, P.; Seelig, J. Structure of Escherichia coli membranes. Glycerol auxotrophs as a tool for the analysis of the phospholipid head-group region by deuterium magnetic resonance Biochemistry 1981, 20, 1826-1831 10.1021/bi00510a017
27. Scherer, P.; Seelig, J. Structure and dynamics of the phosphatidylcholine and the phosphatidylethanolamine head group in L-M fibroblasts as studied by deuterium nuclear magnetic resonance EMBO J. 1987, 6, 2915-2922
28. Shinoda, W.; Namiki, N.; Okazaki, S. Molecular dynamics study of a lipid bilayer: Convergence, structure, and long-time dynamics J. Chem. Phys. 1997, 106, 5731-5743 10.1063/1.473592
29. Högberg, C.-J.; Nikitin, A. M.; Lyubartsev, A. P. Modification of the CHARMM force field for DMPC lipid bilayer J. Comput. Chem. 2008, 29, 2359-2369 10.1002/jcc.20974
30. Castro, V.; Stevensson, B.; Dvinskikh, S. V.; Högberg, C.-J.; Lyubartsev, A. P.; Zimmermann, H.; Sandström, D.; Maliniak, A. NMR investigations of interactions between anesthetics and lipid bilayers Biochim. Biophys. Acta, Biomembr. 2008, 1778, 2604-2611 10.1016/j.bbamem.2008.07.023
31. Klauda, J. B.; Venable, R. M.; Freites, J. A.; OConnor, J. W.; Tobias, D. J.; Mondragon-Ramirez, C.; Vorobyov, I.; MacKerrell, 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 10.1021/jp101759q
32. Kapla, J.; Stevensson, B.; Dahlberg, M.; Maliniak, A. Molecular Dynamics Simulations of Membranes Composed of Glycolipids and Phospholipids J. Phys. Chem. B 2012, 116, 244-252 10.1021/jp209268p
33. Dickson, C. J.; Rosso, L.; Betz, R. M.; Walker, R. C.; Gould, I. R. GAFFlipid: a General Amber Force Field for the accurate molecular dynamics simulation of phospholipid Soft Matter 2012, 8, 9617-9627 10.1039/c2sm26007g
34. Poger, D.; Mark, A. E. Lipid Bilayers: The Effect of Force Field on Ordering and Dynamics J. Chem. Theory Comput. 2012, 8, 4807-4817 10.1021/ct300675z
35. Ferreira, T. M.; Coreta-Gomes, F.; Ollila, O. H. S.; Moreno, M. J.; Vaz, W. L. C.; Topgaard, D. Cholesterol and POPC segmental order parameters in lipid membranes: solid state 1H-13C NMR and MD simulation studies Phys. Chem. Chem. Phys. 2013, 15, 1976-1989 10.1039/C2CP42738A
36. Chowdhary, J.; Harder, E.; Lopes, P. E. M.; Huang, L.; MacKerell, A. D.; Roux, B. A Polarizable Force Field of Dipalmitoylphosphatidylcholine Based on the Classical Drude Model for Molecular Dynamics Simulations of Lipids J. Phys. Chem. B 2013, 117, 9142-9160 10.1021/jp402860e
37. Maciejewski, A.; Pasenkiewicz-Gierula, M.; Cramariuc, O.; Vattulainen, I.; Rog, T. Refined OPLS All-Atom Force Field for Saturated Phosphatidylcholine Bilayers at Full Hydration J. Phys. Chem. B 2014, 118, 4571-4581 10.1021/jp5016627
38. Robinson, A.; Richards, W.; Thomas, P.; Hann, M. Head group and chain behavior in biological membranes: a molecular dynamics computer simulation Biophys. J. 1994, 67, 2345-2354 10.1016/S0006-3495(94)80720-9
39. Essex, J. W.; Hann, M. M.; Richards, W. G. Molecular Dynamics Simulation of a Hydrated Phospholipid Bilayer Philos. Trans. R. Soc., B 1994, 344, 239-260 10.1098/rstb.1994.0064
40. Kothekar, V. Molecular dynamics simulation of hydrated phospholipid bilayers Ind. J. Biochem. Biophys. 1996, 33, 431-447
41. Hyvönen, M. T.; Rantala, T. T.; Ala-Korpela, M. Structure and Dynamic Properties of Diunsaturated 1-Palmitoyl-2-Linoleoyl-sn-Glycero-3-Phosphatidylcholine Lipid Bilayer from Molecular Dynamics Simulation Biophys. J. 1997, 73, 2907-2923 10.1016/S0006-3495(97)78319-X
42. Duong, T. H.; Mehler, E. L.; Weinstein, H. Molecular Dynamics Simulation of Membranes and a Transmembrane Helix J. Comput. Phys. 1999, 151, 358-387 10.1006/jcph.1999.6222
43. Prakash, P.; Sankararamakrishnan, R. Force field dependence of phospholipid headgroup and acyl chain properties: Comparative molecular dynamics simulations of DMPC bilayers J. Comput. Chem. 2010, 31, 266-277 10.1002/jcc.21313
44. 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 10.1016/S0006-3495(97)78845-3
45. Bechinger, B.; Seelig, J. Conformational changes of the phosphatidylcholine headgroup due to membrane dehydration. A 2H-NMR study Chem. Phys. Lipids 1991, 58, 1-5 10.1016/0009-3084(91)90105-K
46. Ulrich, A.; Watts, A. Molecular response of the lipid headgroup to bilayer hydration monitored by 2H-NMR Biophys. J. 1994, 66, 1441-1449 10.1016/S0006-3495(94)80934-8
47. Dvinskikh, S. V.; Castro, V.; Sandstrom, D. Probing segmental order in lipid bilayers at variable hydration levels by amplitude- and phase-modulated cross-polarization NMR Phys. Chem. Chem. Phys. 2005, 7, 3255-3257 10.1039/b508190d
48. Brown, M. F.; Seelig, J. Influence of cholesterol on the polar region of phosphatidylcholine and phosphatidylethanolamine bilayers Biochemistry 1978, 17, 381-384 10.1021/bi00595a029
49. Brown, M. F.; Seelig, J. Ion-induced changes in head group conformation of lecithin bilayers Nature 1977, 269, 721-723 10.1038/269721a0
50. Akutsu, H.; Seelig, J. Interaction of metal ions with phosphatidylcholine bilayer membranes Biochemistry 1981, 20, 7366-7373 10.1021/bi00529a007
51. Altenbach, C.; Seelig, J. Calcium binding to phosphatidylcholine bilayers as studied by deuterium magnetic resonance. Evidence for the formation of a calcium complex with two phospholipid molecules Biochemistry 1984, 23, 3913-3920 10.1021/bi00312a019
52. Roux, M.; Bloom, M. Calcium, magnesium, lithium, sodium, and potassium distributions in the headgroup region of binary membranes of phosphatidylcholine and phosphatidylserine as seen by deuterium NMR Biochemistry 1990, 29, 7077-7089 10.1021/bi00482a019
53. Roux, M.; Bloom, M. Calcium binding by phosphatidylserine headgroups. Deuterium NMR study Biophys. J. 1991, 60, 38-44 10.1016/S0006-3495(91)82028-8
54. Gally, H. U.; Niederberger, W.; Seelig, J. Conformation and motion of the choline head group in bilayers of dipalmitoyl-3-sn-phosphatidylcholine Biochemistry 1975, 14, 3647-3652 10.1021/bi00687a021
55. Scherer, P. G.; Seelig, J. Electric charge effects on phospholipid headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles Biochemistry 1989, 28, 7720-7728 10.1021/bi00445a030
56. Browning, J. L.; Akutsu, H. Local anesthetics and divalent cations have the same effect on the headgroups of phosphatidylcholine and phosphatidylethanolamine Biochim. Biophys. Acta, Biomembr. 1982, 684, 172-178 10.1016/0005-2736(82)90002-5
57. Kelusky, E. C.; Smith, I. C. The influence of local anesthetics on molecular organization in phosphatidylethanolamine membranes Mol. Pharmacol. 1984, 26, 314-321
58. Roux, M.; Neumann, J. M.; Hodges, R. S.; Devaux, P. F.; Bloom, M. Conformational changes of phospholipid headgroups induced by a cationic integral membrane peptide as seen by deuterium magnetic resonance Biochemistry 1989, 28, 2313-2321 10.1021/bi00431a050
59. Kuchinka, E.; Seelig, J. Interaction of melittin with phosphatidylcholine membranes. Binding isotherm and lipid head-group conformation Biochemistry 1989, 28, 4216-4221 10.1021/bi00436a014
60. Catte, A.; Girych, M.; Javanainen, M.; Miettinen, M. S.; Monticelli, L.; Määttä, J.; Oganesyan, V. S.; Ollila, O. H. S. Electrometer concept and binding of cations to phospholipid bilayers 2015, 10.5281/zenodo.32175
61. Miettinen, S. M.; Ollila, O. H. S.; Botan, A.; Catte, A.; Edholm, O.; Favela, F.; Ferreira, T.; Fuchs, P.; Girych, M. et al. NMRLipids project 2015, 10.6084/m9.figshare.1585017
62. Gowers, T.; Nielsen, M. Massively collaborative mathematics Nature 2009, 461, 879-881 10.1038/461879a
63. Ollila, O. H. S. Response of the hydrophilic part of lipid membranes to changing conditions-a critical comparison of simulations to experiments. 2013; http://arxiv.org/abs/1309.2131v1.
64. Ollila, S.; Miettinen, S. M. On credits 2015, 10.6084/m9.figshare.1577577
65. Botan, A.; Favela-Rosales, F.; Fuchs, P. F. J.; Javanainen, M.; Kanduč, M.; Kulig, W.; Lamberg, A.; Loison, C.; Lyubartsev, A.; Miettinen, M. S. et al. nmrlipids.blogspot.fi: Final submission to the J. Phys. Chem. B 2015, 10.5281/zenodo.32689
66. Seelig, J. Deuterium magnetic resonance: theory and application to lipid membranes Q. Rev. Biophys. 1977, 10, 353-418 10.1017/S0033583500002948
67. Hong, M.; Schmidt-Rohr, K.; Pines, A. NMR Measurement of Signs and Magnitudes of C-H Dipolar Couplings in Lecithin J. Am. Chem. Soc. 1995, 117, 3310-3311 10.1021/ja00116a051
68. Gross, J. D.; Warschawski, D. E.; Griffin, R. G. Dipolar Recoupling in MAS NMR: A Probe for Segmental Order in Lipid Bilayers J. Am. Chem. Soc. 1997, 119, 796-802 10.1021/ja962951b
69. Dvinskikh, S. V.; Castro, V.; Sandstrom, D. Efficient solid-state NMR methods for measuring heteronuclear dipolar couplings in unoriented lipid membrane systems Phys. Chem. Chem. Phys. 2005, 7, 607-613 10.1039/b418131j
70. Ollila, S.; Miettinen, S. M.; Vogel, A. Accuracy of order parameter measurements 2015, 10.6084/m9.figshare.1577576
71. Ollila, S.; Fuchs, P.; Javanainen, M.; Lamberg, A. On the signs of the order parameters 2015, 10.6084/m9.figshare.1577578
72. Engel, A. K.; Cowburn, D. The origin of multiple quadrupole couplings in the deuterium NMR spectra of the 2 chain of 1,2 dipalmitoyl-sn-glycero-3-phosphorylcholine FEBS Lett. 1981, 126, 169-171 10.1016/0014-5793(81)80233-5
73. Vogel, A.; Feller, S. Headgroup Conformations of Phospholipids from Molecular Dynamics Simulation: Sampling Challenges and Comparison to Experiment J. Membr. Biol. 2012, 245, 23-28 10.1007/s00232-011-9411-5
74. Ollila, S.; Hyvönen, M. T.; Vattulainen, I. Polyunsaturation in Lipid Membranes: Dynamic Properties and Lateral Pressure Profiles J. Phys. Chem. B 2007, 111, 3139-3150 10.1021/jp065424f
75. Ferreira, T. M.; Ollila, O. H. S.; Pigliapochi, R.; Dabkowska, A. P.; Topgaard, D. Model-free estimation of the effective correlation time for CH bond reorientation in amphiphilic bilayers: 1H13C solid-state NMR and MD simulations J. Chem. Phys. 2015, 142, 044905 10.1063/1.4906274
76. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447 10.1021/ct700301q
77. Plimpton, S. Fast Parallel Algorithms for Short-Range Molecular Dynamics J. Comput. Phys. 1995, 117, 1-19 10.1006/jcph.1995.1039
78. Lyubartsev, A. P.; Laaksonen, A. M. DynaMix a scalable portable parallel MD simulation package for arbitrary molecular mixtures Comput. Phys. Commun. 2000, 128, 565-589 10.1016/S0010-4655(99)00529-9
79. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable molecular dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802 10.1002/jcc.20289
80. Gurtovenko, A. A.; Patra, M.; Karttunen, M.; Vattulainen, I. Cationic DMPC/DMTAP Lipid Bilayers: Molecular Dynamics Study Biophys. J. 2004, 86, 3461-3472 10.1529/biophysj.103.038760
81. Miettinen, M. S. Molecular dynamics simulation trajectory of a fully hydrated DMPC lipid bilayer 2013, 10.6084/m9.figshare.829642
82. Miettinen, M. S.; Gurtovenko, A. A.; Vattulainen, I.; Karttunen, M. Ion Dynamics in Cationic Lipid Bilayer Systems in Saline Solutions J. Phys. Chem. B 2009, 113, 9226-9234 10.1021/jp810233q
83. Marrink, S.-J.; Berger, O.; Tieleman, P.; Jähnig, F. Adhesion Forces of Lipids in a Phospholipid Membrane Studied by Molecular Dynamics Simulations Biophys. J. 1998, 74, 931-943 10.1016/S0006-3495(98)74016-0
84. Määttä, J. DPPC-Berger. 2015; DOI: 10.5281/zenodo.13934
85. Ollila, O. H. S.; Ferreira, T.; Topgaard, D. MD simulation trajectory and related files for POPC bilayer (Berger model delivered by Tieleman, Gromacs 4.5). 2014; DOI: 10.5281/zenodo.13279.
86. Ollila, O. H. S.; Miettinen, M. MD simulation trajectory and related files for DPPC bilayer (CHARMM36, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.15549.
87. Ollila, O. H. S.; Miettinen, M. MD simulation trajectory and related files for POPC bilayer (CHARMM36, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.13944.
88. Santuz, H. MD simulation trajectory and related files for POPC bilayer (CHARMM36, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.14066.
89. Kulig, W.; Pasenkiewicz-Gierula, M.; Róg, T. Cis and Trans Unsaturated Phosphatidylcholine Bilayers: A Molecular Dynamics Simulation Study Chem. Phys. Lipids 2016, 195, 12-20 10.1016/j.chemphyslip.2015.07.002
90. Javanainen, M. POPC @ 310K, model by Maciejewski and Rog. 2014; DOI: 10.5281/zenodo.13497.
91. Javanainen, M. POPC/Cholesterol @ 310K, 0, 10, 40, 50 and 60 mol-% cholesterol. Model by Maciejewski and Rog. 2015; DOI: 10.5281/zenodo.13877.
92. Javanainen, M. POPC @ 310K, varying water-to-lipid ratio. Model by Maciejewski and Rog. 2014; DOI: 10.5281/zenodo.13498.
93. Ollila, O. H. S.; Retegan, M. MD simulation trajectory and related files for DPPC bilayer (GAFFlipid, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.15550.
94. Ollila, O. H. S.; Retegan, M. MD simulation trajectory and related files for POPC bilayer (GAFFlipid, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.13791.
95. Dickson, C. J.; Madej, B. D.; Skjevik, g. 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 10.1021/ct4010307
96. Ollila, O. H. S.; Retegan, M. MD simulation trajectory and related files for POPC bilayer (Lipid14, Gromacs 4.5). 2014; DOI: 10.5281/zenodo.12767.
97. Poger, D.; Van Gunsteren, W. F.; Mark, A. E. A new force field for simulating phosphatidylcholine bilayers J. Comput. Chem. 2010, 31, 1117-1125 10.1002/jcc.21396
98. Fuchs, P. F. MD simulation trajectory and related files for DPPC bilayer in full hydration (Poger GROMOS53A6-L, Gromacs 4.0.7, PME, traj 1). 2015; DOI: 10.5281/zenodo.14594
99. Fuchs, P. F. MD simulation trajectory and related files for DPPC bilayer in full hydration (Poger GROMOS53A6-L, Gromacs 4.0.7, PME, traj 2). 2015; DOI: 10.5281/zenodo.14595
100. 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 10.1021/jp212503e
101. Määttä, J. DPPC-Slipids. 2014; DOI: 10.5281/zenodo.13287
102. 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 10.1021/ct300342n
103. Javanainen, M. POPC @ 310K, Slipids force field. 2015; DOI: 10.5281/zenodo.13887.
104. Kukol, A. Lipid Models for United-Atom Molecular Dynamics Simulations of Proteins J. Chem. Theory Comput. 2009, 5, 615-626 10.1021/ct8003468
105. Javanainen, M. POPC @ 298K, Model by Kukol. 2014; DOI: 10.5281/zenodo.13393.
106. 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 10.1021/jp807056c
107. Ollila, O. H. S. MD simulation trajectory and related files for POPC bilayer (Chiu et al. Gromos version, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.15548.
108. Lyubartsev, A. et al. MD simulation trajectory and related files for DMPC bilayer, Högberg J. Comput. Chem. 2008, 29, 2359 10.5281/zenodo.16195
109. Rabinovich, A. L.; Lyubartsev, A. P. Bond orientation properties in lipid molecules of membranes: molecular dynamics simulations J. Phys.: Conf. Ser. 2014, 510, 012022 10.1088/1742-6596/510/1/012022
110. Lyubartsev, A. MD simulation trajectory and related files for POPC bilayer, Högberg et al parameters J. Comput. Chem. 2008, 29, 2359 10.5281/zenodo.16724
111. Ulmschneider, J. P.; Ulmschneider, M. B. United Atom Lipid Parameters for Combination with the Optimized Potentials for Liquid Simulations All-Atom Force Field J. Chem. Theory Comput. 2009, 5, 1803-1813 10.1021/ct900086b
112. Javanainen, M. POPC @ 310K, Model by Ulmschneider and Ulmschneider. 2014; DOI: 10.5281/zenodo.13392.
113. Tjörnhammar, R.; Edholm, O. Reparameterized United Atom Model for Molecular Dynamics Simulations of Gel and Fluid Phosphatidylcholine Bilayers J. Chem. Theory Comput. 2014, 10, 5706-5715 10.1021/ct500589z
114. Javanainen, M. DPPC @ 323K, new FF by Tjörnhammar and Edholm. 2014; DOI: 10.5281/zenodo.12743.
115. Henin, J.; Shinoda, W.; Klein, M. L. United-Atom Acyl Chains for CHARMM Phospholipids J. Phys. Chem. B 2008, 112, 7008-7015 10.1021/jp800687p
116. Botan, A. DLPC @ 323K, CHARMM36UA force field. 2015; DOI: 10.5281/zenodo.13821.
117. 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 10.1021/jp410344g
118. Loison, C. Hydrated DPPC, MD simulation trajectory and related files for UA charmm36 model by Lee et al 2014. 2015; DOI: 10.5281/zenodo.17004.
119. Ollila, O. H. S. MD simulation trajectory and related files for POPC bilayer in low hydration (Berger model delivered by Tieleman, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.13814.
120. Kanduč, M.; Schneck, E.; Netz, R. R. Hydration Interaction between Phospholipid Membranes: Insight into Different Measurement Ensembles from Atomistic Molecular Dynamics Simulations Langmuir 2013, 29, 9126-9137 10.1021/la401147b
121. Kanduc, M. MD trajectory for DLPC bilayer (Berger, Gromacs 4.5.4), nw/28 w/l. 2015; DOI: 10.5281/zenodo.16287.
122. Kanduc, M. MD trajectory for DLPC bilayer (Berger, Gromacs 4.5.4), nw/24 w/l. 2015; DOI: 10.5281/zenodo.16289.
123. Kanduc, M. MD trajectory for DLPC bilayer (Berger, Gromacs 4.5.4), nw/20 w/l. 2015; DOI: 10.5281/zenodo.16291.
124. Kanduc, M. MD trajectory for DLPC bilayer (Berger, Gromacs 4.5.4), nw/16 w/l. 2015; DOI: 10.5281/zenodo.16292.
125. Kanduc, M. MD trajectory for DLPC bilayer (Berger, Gromacs 4.5.4), nw/12 w/l. 2015; DOI: 10.5281/zenodo.16293.
126. Kanduc, M. MD trajectory for DLPC bilayer (Berger, Gromacs 4.5.4), nw/8 w/l. 2015; DOI: 10.5281/zenodo.16294.
127. Kanduc, M. MD trajectory for DLPC bilayer (Berger, Gromacs 4.5.4), nw/4 w/l. 2015; DOI: 10.5281/zenodo.16295.
128. Ollila, O. H. S.; Miettinen, M. MD simulation trajectory and related files for POPC bilayer in medium low hydration (CHARMM36, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.13946.
129. Ollila, O. H. S.; Miettinen, M. MD simulation trajectory and related files for POPC bilayer in low hydration (CHARMM36, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.13945.
130. Ollila, O. H. S. MD simulation trajectory and related files for POPC bilayer in low hydration (GAFFlipid, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.13853.
131. Höltje, M.; Förster, T.; Brandt, B.; Engels, T.; von Rybinski, W.; Höltje, H.-D. Molecular dynamics simulations of stratum corneum lipid models: fatty acids and cholesterol Biochim. Biophys. Acta, Biomembr. 2001, 1511, 156-167 10.1016/S0005-2736(01)00270-X
132. Ollila, O. H. S.; Ferreira, T.; Topgaard, D. MD simulation trajectory and related files for POPC/cholesterol (7 mol%) bilayer (Berger model delivered by Tieleman, modified Höltje, Gromacs 4.5). 2014; DOI: 10.5281/zenodo.13282.
133. Ollila, O. H. S.; Ferreira, T.; Topgaard, D. MD simulation trajectory and related files for POPC/cholesterol (15 mol%) bilayer (Berger model delivered by Tieleman, modified Höltje, Gromacs 4.5). 2014; DOI: 10.5281/zenodo.13281.
134. Ollila, O. H. S.; Ferreira, T.; Topgaard, D. MD simulation trajectory and related files for POPC/cholesterol (34 mol%) bilayer (Berger model delivered by Tieleman, modified Höltje, Gromacs 4.5). 2014; DOI: 10.5281/zenodo.13283.
135. Ollila, O. H. S.; Ferreira, T.; Topgaard, D. MD simulation trajectory and related files for POPC/cholesterol (50 mol%) bilayer (Berger model delivered by Tieleman, modified Höltje, Gromacs 4.5). 2014; DOI: 10.5281/zenodo.13285.
136. Ollila, O. H. S.; Ferreira, T.; Topgaard, D. MD simulation trajectory and related files for POPC/cholesterol (60 mol%) bilayer (Berger model delivered by Tieleman, modified Höltje, Gromacs 4.5). 2014; DOI: 10.5281/zenodo.13286.
137. Lim, J. B.; Rogaski, B.; Klauda, J. B. Update of the Cholesterol Force Field Parameters in CHARMM J. Phys. Chem. B 2012, 116, 203-210 10.1021/jp207925m
138. Favela-Rosales, F. POPC-Glycerol-CHARMM36-0-10-15-20-25-35-50%CHOL. 2015; DOI: 10.5281/zenodo.16830.
139. Santuz, H. MD simulation trajectory for POPC/20% Chol bilayer (CHARMM36, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.14067.
140. Santuz, H. MD simulation trajectory for POP @ C/50% Chol bilayer (CHARMM36, Gromacs 4.5). 2015; DOI: 10.5281/zenodo.14068.
141. Warschawski, D.; Devaux, P. Order parameters of unsaturated phospholipids in membranes and the effect of cholesterol: a 1H-13C solid-state NMR study at natural abundance Eur. Biophys. J. 2005, 34, 987-996 10.1007/s00249-005-0482-z
142. Mashl, R. J.; Scott, H. L.; Subramaniam, S.; Jakobsson, E. Molecular Simulation of Dioleoylphosphatidylcholine Lipid Bilayers at Differing Levels of Hydration Biophys. J. 2001, 81, 3005-3015 10.1016/S0006-3495(01)75941-3
143. Pertsin, A.; Platonov, D.; Grunze, M. Direct computer simulation of water-mediated force between supported phospholipid membranes J. Chem. Phys. 2005, 122, 244708 10.1063/1.1940568
144. Pertsin, A.; Platonov, D.; Grunze, M. Origin of Short-Range Repulsion between Hydrated Phospholipid Bilayers:? A Computer Simulation Study Langmuir 2007, 23, 1388-1393 10.1021/la0622929
145. Eun, C.; Berkowitz, M. L. Origin of the Hydration Force: Water-Mediated Interaction between Two Hydrophilic Plates J. Phys. Chem. B 2009, 113, 13222-13228 10.1021/jp901747s
146. Eun, C.; Berkowitz, M. L. Thermodynamic and Hydrogen-Bonding Analyses of the Interaction between Model Lipid Bilayers J. Phys. Chem. B 2010, 114, 3013-3019 10.1021/jp910347n
147. Schneck, E.; Sedlmeier, F.; Netz, R. R. Hydration repulsion between biomembranes results from an interplay of dehydration and depolarization Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 14405-14409 10.1073/pnas.1205811109
148. Israelachvili, J. N. Intermolecular and Surface Forces; Academic Press: London, 1985.
149. Israelachvili, J. N.; Wennerström, H. Role of hydration and water structure in biological and colloidal interactions Nature 1996, 379, 219-225 10.1038/379219a0
150. Sparr, E.; Wennerström, H. Interlamellar forces and the thermodynamic characterization of lamellar phospholipid systems Curr. Opin. Colloid Interface Sci. 2011, 16, 561-567 10.1016/j.cocis.2011.05.003
151. Simons, K.; Vaz, W. L. Model Systems, Lipid Rafts, And Cell Membranes Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 269-295 10.1146/annurev.biophys.32.110601.141803
152. Somerharju, P.; Virtanen, J. A.; Cheng, K. H.; Hermansson, M. The superlattice model of lateral organization of membranes and its implications on membrane lipid homeostasis Biochim. Biophys. Acta, Biomembr. 2009, 1788, 12-23 10.1016/j.bbamem.2008.10.004
153. Huang, J.; Feigenson, G. W. A Microscopic Interaction Model of Maximum Solubility of Cholesterol in Lipid Bilayers Biophys. J. 1999, 76, 2142-2157 10.1016/S0006-3495(99)77369-8
154. Zhu, Q.; Cheng, K. H.; Vaughn, M. W. Molecular Dynamics Studies of the Molecular Structure and Interactions of Cholesterol Superlattices and Random Domains in an Unsaturated Phosphatidylcholine Bilayer Membrane J. Phys. Chem. B 2007, 111, 11021-11031 10.1021/jp070487z
155. Róg, T.; Pasenkiewicz-Gierula, M.; Vattulainen, I.; Karttunen, M. Ordering effects of cholesterol and its analogues Biochim. Biophys. Acta, Biomembr. 2009, 1788, 97-121 10.1016/j.bbamem.2008.08.022
156. Alwarawrah, M.; Dai, J.; Huang, J. Modification of Lipid Bilayer Structure by Diacylglycerol: A Comparative Study of Diacylglycerol and Cholesterol J. Chem. Theory Comput. 2012, 8, 749-758 10.1021/ct200790q
157. Marsh, D. Liquid-ordered phases induced by cholesterol: A compendium of binary phase diagrams Biochim. Biophys. Acta, Biomembr. 2010, 1798, 688-699 10.1016/j.bbamem.2009.12.027
158. Ghosh, R.; Seelig, J. The interaction of cholesterol with bilayers of phosphatidylethanolamine Biochim. Biophys. Acta, Biomembr. 1982, 691, 151-160 10.1016/0005-2736(82)90224-3
159. Ferreira, T. M.; Topgaard, D.; Ollila, O. H. S. Molecular Conformation and Bilayer Pores in a Nonionic Surfactant Lamellar Phase Studied with 1H13C Solid-State NMR and Molecular Dynamics Simulations Langmuir 2014, 30, 461-469 10.1021/la404684r