Combination of MD Simulations with Two-State Kinetic Rate Modeling Elucidates the Chain Melting Transition of Phospholipid Bilayers for Different Hydration Levels

Journal of Physical Chemistry B

Volumn 119, Issue 44, 2015, Pages 14157-14167

  Kowalik, Bartosz ^a   Schubert, Thomas ^b   Wada, Hirofumi ^c   Tanaka, Motomu ^b,d   Netz, Roland R ^a   Schneck, Emanuel ^e  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c RITSUMEIKAN UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CHAINS; CYTOLOGY; HYDRATION; LIPIDS; MELTING; MEMBRANES; MOLECULAR DYNAMICS; PHOSPHOLIPIDS;

ATOMISTIC MOLECULAR DYNAMICS SIMULATIONS; CHAIN MELTING TRANSITION; DIPALMITOYL PHOSPHATIDYLCHOLINE; EQUILIBRIUM MELTING TEMPERATURE; MOLECULAR TRANSPORT; PHOSPHOLIPID BILAYER; THERMODYNAMIC QUANTITIES; VARIABLE HEATING RATES;

PHASE TRANSITIONS;

LIPID BILAYER; PHOSPHOLIPID;

CHEMISTRY; DEHYDRATION; KINETICS; LIPID BILAYER; MOLECULAR DYNAMICS; OSMOTIC PRESSURE; THERMODYNAMICS;

DEHYDRATION; KINETICS; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; OSMOTIC PRESSURE; PHOSPHOLIPIDS; THERMODYNAMICS;

EID: 84946594363     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b05501     Document Type: Article

References (67)

1. Singer, S. J.; Nicolson, G. L. The fluid mosaic model of the structure of cell membranes Science 1972, 175, 720-731 10.1126/science.175.4023.720
2. Cevc, G.; Marsh, D. Phospholipid bilayers: physical principles and models; Wiley, 1987; Vol. 5.
3. Lipowsky, R.; Sackmann, E. Structure and Dynamics of Membranes: I. From Cells to Vesicles/II. Generic and Specific Interactions; Access Online via Elsevier, 1995; Vol. 1.
4. Mouritsen, O. G. Life-As a Matter of Fat; Springer, 2005.
5. Bloom, M.; Evans, E.; Mouritsen, O. G. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective Q. Rev. Biophys. 1991, 24, 293-397 10.1017/S0033583500003735
6. Sparr, E.; Wennerström, H. Responding phospholipid membranes-interplay between hydration and permeability Biophys. J. 2001, 81, 1014-1028 10.1016/S0006-3495(01)75759-1
7. Nagle, J. F.; Tristram-Nagle, S. Structure of lipid bilayers Biochim. Biophys. Acta, Rev. Biomembr. 2000, 1469, 159 10.1016/S0304-4157(00)00016-2
8. Kucerka, N.; Tristram-Nagle, S.; Nagle, J. F. Closer Look at Structure of Fully Hydrated Fluid Phase DPPC Bilayers Biophys. J. 2006, 90, L83 10.1529/biophysj.106.086017
9. Tristram-Nagle, S.; Zhang, R.; Suter, R.; Worthington, C.; Sun, W.; Nagle, J. Measurement of chain tilt angle in fully hydrated bilayers of gel phase lecithins Biophys. J. 1993, 64, 1097-1109 10.1016/S0006-3495(93)81475-9
10. Biltonen, R. L. A statistical-thermodynamic view of cooperative structural changes in phospholipid bilayer membranes: their potential role in biological function J. Chem. Thermodyn. 1990, 22, 1-19 10.1016/0021-9614(90)90026-M
11. Mabrey, S.; Sturtevant, J. M. Investigation of phase transitions of lipids and lipid mixtures by high sensitivity differential scanning calorimetry Proc. Natl. Acad. Sci. U. S. A. 1976, 73, 3862-3866 10.1073/pnas.73.11.3862
12. Janiak, M. J.; Small, M. D.; Shipley, G. G. Nature of the thermal pretransition of synthetic phospholipids: dimyristoyl- and dipalmitoyllecithin Biochemistry 1976, 15, 4575 10.1021/bi00666a005
13. Koynova, R.; Caffrey, M. Phases and phase transitions of the phosphatidylcholines Biochim. Biophys. Acta, Rev. Biomembr. 1998, 1376, 91-145 10.1016/S0304-4157(98)00006-9
14. Jürgens, E.; Höhne, G.; Sackmann, E. Calorimetric Study of the Dipalmitoylphosphatidylcholine/ Water Phase Diagram Ber. Bunsenges. Phys. Chem. 1983, 87, 95-104 10.1002/bbpc.19830870207
15. Grabielle-Madelmont, C.; Perron, R. Calorimetric studies on phospholipid-water systems: I. dl-Dipalmitoylphosphatidylcholine (DPPC)-water system J. Colloid Interface Sci. 1983, 95, 471-482 10.1016/0021-9797(83)90207-2
16. Costa-Balogh, F. O.; Wennerström, H.; Wadsö, L.; Sparr, E. How small polar molecules protect membrane systems against osmotic stress: the urea-water-phospholipid system J. Phys. Chem. B 2006, 110, 23845-23852 10.1021/jp0632440
17. Kharakoz, D.; Colotto, A.; Lohner, K.; Laggner, P. Fluid-gel interphase line tension and density fluctuations in dipalmitoylphosphatidylcholine multilamellar vesicles: an ultrasonic study J. Phys. Chem. 1993, 97, 9844-9851 10.1021/j100140a049
18. Kharakoz, D. P.; Shlyapnikova, E. A. Thermodynamics and kinetics of the early steps of solid-state nucleation in the fluid lipid bilayer J. Phys. Chem. B 2000, 104, 10368-10378 10.1021/jp001299a
19. Frenkel, J. A general theory of heterophase fluctuations and pretransition phenomena J. Chem. Phys. 1939, 7, 538 10.1063/1.1750484
20. Spaepen, F. Homogeneous nucleation and the temperature dependence of the crystalmelt interfacial tension Solid State Phys. 1994, 47, 1 10.1016/S0081-1947(08)60638-4
21. Vehkamäki, H. Classical nucleation theory in multicomponent systems; Springer: Berlin Heidelberg, 2006.
22. Mouritsen, O. Theoretical models of phospholipid phase transitions Chem. Phys. Lipids 1991, 57, 179-194 10.1016/0009-3084(91)90075-M
23. Nagle, J. F. Theory of the main lipid bilayer phase transition Annu. Rev. Phys. Chem. 1980, 31, 157-196 10.1146/annurev.pc.31.100180.001105
24. Mouritsen, O.; Boothroyd, A.; Harris, R.; Jan, N.; Lookman, T.; MacDonald, L.; Pink, D.; Zuckermann, M. Computer simulation of the main gel-fluid phase transition of lipid bilayers J. Chem. Phys. 1983, 79, 2027 10.1063/1.445987
25. Jämbeck, J. P.; 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
26. Marrink, S.-J.; Berendsen, H. J. Simulation of water transport through a lipid membrane J. Phys. Chem. 1994, 98, 4155-4168 10.1021/j100066a040
27. de Vries, A. H.; Chandrasekhar, I.; van Gunsteren, W. F.; Hünenberger, P. H. Molecular dynamics simulations of phospholipid bilayers: Influence of artificial periodicity, system size, and simulation time J. Phys. Chem. B 2005, 109, 11643-11652 10.1021/jp0507952
28. 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
29. Leekumjorn, S.; Sum, A. K. Molecular studies of the gel to liquid-crystalline phase transition for fully hydrated DPPC and DPPE bilayers Biochim. Biophys. Acta, Biomembr. 2007, 1768, 354-365 10.1016/j.bbamem.2006.11.003
30. Schubert, T.; Schneck, E.; Tanaka, M. First Order Melting Transitions of Highly Ordered DPPC Gel Phase Membranes in Molecular Dynamics Simulations with Atomistic Detail J. Chem. Phys. 2011, 135, 055105 10.1063/1.3615937
31. Venable, R. M.; Brooks, B. R.; Pastor, R. W. Molecular dynamics simulations of gel (LβI) phase lipid bilayers in constant pressure and constant surface area ensembles J. Chem. Phys. 2000, 112, 4822-4832 10.1063/1.481085
32. Coppock, P. S.; Kindt, J. T. Atomistic simulations of mixed-lipid bilayers in gel and fluid phases Langmuir 2009, 25, 352-359 10.1021/la802712q
33. Coppock, P. S.; Kindt, J. T. Determination of phase transition temperatures for atomistic models of lipids from temperature-dependent stripe domain growth kinetics J. Phys. Chem. B 2010, 114, 11468-11473 10.1021/jp104529m
34. Geiger, P.; Dellago, C. Neural networks for local structure detection in polymorphic systems J. Chem. Phys. 2013, 139, 164105 10.1063/1.4825111
35. Kumar, S.; Rosenberg, J. M.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 1992, 13, 1011-1021 10.1002/jcc.540130812
36. Chung, H. S.; Louis, J. M.; Eaton, W. A. Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 11837-11844 10.1073/pnas.0901178106
37. Onuchic, J. N.; Luthey-Schulten, Z.; Wolynes, P. G. Theory of protein folding: the energy landscape perspective Annu. Rev. Phys. Chem. 1997, 48, 545-600 10.1146/annurev.physchem.48.1.545
38. Godoy-Ruiz, R.; Henry, E. R.; Kubelka, J.; Hofrichter, J.; Munoz, V.; Sanchez-Ruiz, J. M.; Eaton, W. A. Estimating free-energy barrier heights for an ultrafast folding protein from calorimetric and kinetic data J. Phys. Chem. B 2008, 112, 5938-5949 10.1021/jp0757715
39. 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 10.1021/ct700301q
40. Tieleman, D.; Berendsen, H. J. C. Molecular dynamics simulations of a fully hydrated dipalmitoyl phosphatidylcholine bilayer with different macroscopic boundary conditions and parameters J. Chem. Phys. 1996, 105, 4871 10.1063/1.472323
41. 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 10.1016/S0006-3495(97)78845-3
42. Lindahl, E.; Edholm, O. Mesoscopic Undulations and Thickness Fluctuations in Lipid Bilayers from Molecular Dynamics Simulations Biophys. J. 2000, 79, 426-433 10.1016/S0006-3495(00)76304-1
43. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926 10.1063/1.445869
44. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684 10.1063/1.448118
45. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N log(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98, 10089 10.1063/1.464397
46. 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 10.1063/1.470117
47. Kissinger, H. E. Reaction kinetics in differential thermal analysis Anal. Chem. 1957, 29, 1702-1706 10.1021/ac60131a045
48. Farjas, J.; Roura, P. Modification of the Kolmogorov-Johnson-Mehl-Avrami rate equation for non-isothermal experiments and its analytical solution Acta Mater. 2006, 54, 5573-5579 10.1016/j.actamat.2006.07.037
49. Corless, R. M.; Gonnet, G. H.; Hare, D. E. G.; Jeffrey, D. J.; Knuth, D. E. On the LambertW function Adv. Comput. Math. 1996, 5, 329-359 10.1007/BF02124750
50. Bell, G. I. Models for the specific adhesion of cells to cells Science 1978, 200, 618 10.1126/science.347575
51. Evans, E.; Ritchie, K. Dynamic strength of molecular adhesion bonds Biophys. J. 1997, 72, 1541 10.1016/S0006-3495(97)78802-7
52. Rief, M.; Gautel, M.; Oesterhelt, F.; Fernandez, J. M.; Gaub, H. E. Reversible Unfolding of Individual Titin Immunoglobulin Domains by AFM Science 1997, 276, 1109 10.1126/science.276.5315.1109
53. Hinz, H.-J.; Sturtevant, J. M. Calorimetric studies of dilute aqueous suspensions of bilayers formed from synthetic L-α-lecithins J. Biol. Chem. 1972, 247, 6071-6075
54. Blume, A. Apparent molar heat capacities of phospholipids in aqueous dispersion. Effects of chain length and head group structure Biochemistry 1983, 22, 5436-5442 10.1021/bi00292a027
55. Sun, W.; Tristram-Nagle, S.; Suter, R. M.; Nagle, J. F. Structure of the ripple phase in lecithin bilayers Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 7008-7012 10.1073/pnas.93.14.7008
56. de Vries, A. H.; Yefimov, S.; Mark, A. E.; Marrink, S. J. Molecular structure of the lecithin ripple phase Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 5392-5396 10.1073/pnas.0408249102
57. Garg, S.; Rühe, J.; Lüdtke, K.; Jordan, R.; Naumann, C. A. Domain Registration in Raft-Mimicking Lipid Mixtures Studied Using Polymer-Tethered Lipid Bilayers Biophys. J. 2007, 92, 1263-1270 10.1529/biophysj.106.091082
58. May, S. Trans-monolayer coupling of fluid domains in lipid bilayers Soft Matter 2009, 5, 3148-3156 10.1039/b901647c
59. Ulminus, J.; Wennerstrom, H.; Lindblom, G.; Arvidson, G. Deuteron nuclear magnetic resonance studies of phase equilibriums in a lecithin-water system Biochemistry 1977, 16, 5742-5745 10.1021/bi00645a014
60. Vega, C.; Abascal, J. L. Simulating water with rigid non-polarizable models: a general perspective Phys. Chem. Chem. Phys. 2011, 13, 19663-19688 10.1039/c1cp22168j
61. Ginnings, D. C.; Furukawa, G. T. Heat Capacity Standards for the Range 14 to 1200 degrees K J. Am. Chem. Soc. 1953, 75, 522-527 10.1021/ja01099a004
62. Bevington, P. R.; Robinson, D. K. Data reduction and error analysis for the physical sciences; McGraw-Hill: New York, 1969; Vol. 336.
63. Parente, R. A.; Lentz, B. R. Phase behavior of large unilamellar vesicles composed of synthetic phospholipids Biochemistry 1984, 23, 2353-2362 10.1021/bi00306a005
64. Guldbrand, L.; Jönsson, B.; Wennerstrom, H. Hydration forces and phase equilibria in the dipalmitoyl phosphatidylcholine-water system J. Colloid Interface Sci. 1982, 89, 532-541 10.1016/0021-9797(82)90204-1
65. Goldstein, R. E.; Leibler, S. Model for Lamellar Phases of Interacting Lipid Membranes Phys. Rev. Lett. 1988, 61, 2213-2216 10.1103/PhysRevLett.61.2213
66. Griesbauer, J.; Bössinger, S.; Wixforth, A.; Schneider, M. Propagation of 2D pressure pulses in lipid monolayers and its possible implications for biology Phys. Rev. Lett. 2012, 108, 198103 10.1103/PhysRevLett.108.198103
67. Kanduc, 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