The limiting behavior of water hydrating a phospholipid monolayer: A computer simulation study

We report molecular dynamics simulations of water hydrating a lipid (dimyristoylphosphatidylcholine) monolayer under conditions chosen to eliminate simulation artifacts. These simulations provide a description of the behavior of the membrane–water interface that agrees with recent experimental studies. In particular, we find that the hydrating water orients to contribute the positive end of its dipole to the substantially positive electrostatic potential of the membrane interior, consistent with interpretations of recent experiments. In addition, recent experiments show that this water reorients rapidly on the NMR time scale. Our results concur, however the relatively rapid water motion does not preclude the preferential ordering that we observe. The limiting behavior of the system shows three hydration shells about the lipid PC headgroups and significant hydrogen bonding of water to the phosphate groups. The choline group experiences different environments, and the structure of the first hydration shell clearly corresponds to a clathrate. The motion of the hydrating water was found to be slower than that of bulk water, and the computed residence times for water about the lipids (20 ps about choline, 10 ps about phosphate) were in excellent agreement with results of NMR experiments. This further shows that water resides in a clathrate shell longer than in a shell about ions. In addition, we show that the structure and dynamics of water hydrating the lipids are very sensitive to the treatment of the long‐range interactions. In particular, the radial structure sharpens considerably, a third hydration shell about the phosphate was observed only with large cutoffs, and hydrogen bonding of water to the lipids increased by 25%. The water moved more slowly than bulk when large cutoffs were employed but moved faster than bulk water when small cutoffs were used and the residence times for water about the lipids were twofold–fivefold larger using large cutoffs. In general it was found that the lipids significantly influence water out to several hydration shells, and that water hydrating the lipids behaves differently than bulk water.

[1]  Anders Wallqvist,et al.  Molecular dynamics study of a hydrophobic aggregate in an aqueous solution of methane , 1991 .

[2]  T. McIntosh,et al.  Magnitude of the solvation pressure depends on dipole potential. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[3]  H. Hauser.  The polar group conformation of 1,2-dialkyl phosphatidylcholines An NMR study , 1981 .

[4]  J. Andrew McCammon,et al.  The structure of liquid water at an extended hydrophobic surface , 1984 .

[5]  W. L. Jorgensen,et al.  Comparison of simple potential functions for simulating liquid water , 1983 .

[6]  E. Clementi,et al.  Structure and Motion: Membranes, Nucleic Acids and Proteins , 1985 .

[7]  Charles L. Brooks,et al.  The influence of long-range force truncation on the thermodynamics of aqueous ionic solutions , 1987 .

[8]  H. Hauser,et al.  Preferred conformation and molecular packing of phosphatidylethanolamine and phosphatidylcholine. , 1981, Biochimica et biophysica acta.

[9]  Ronald M. Levy,et al.  Molecular dynamics simulations of water with Ewald summation for the long range electrostatic interactions , 1991 .

[10]  V. Parsegian,et al.  Measurement of forces between lecithin bilayers , 1976, Nature.

[11]  Keith B. Ward,et al.  Simulations of lipid crystals: Characterization of potential energy functions and parameters for lecithin molecules , 1991 .

[12]  Roger Impey,et al.  Hydration and mobility of ions in solution , 1983 .

[13]  H. Berendsen,et al.  Molecular dynamics with coupling to an external bath , 1984 .

[14]  H. L. Scott,et al.  Density and bonding profiles of interbilayer water as functions of bilayer separation: a Monte Carlo study , 1987 .

[15]  O. Steinhauser,et al.  Taming cut-off induced artifacts in molecular dynamics studies of solvated polypeptides. The reaction field method. , 1992, Journal of molecular biology.

[16]  P. Rossky,et al.  Solvent molecular dynamics in regions of hydrophobic hydration , 1986 .

[17]  Studies on membrane hydration.: Part I. Monte Carlo simulation of the cholesterol—water interface , 1987 .

[18]  G. W. Robinson,et al.  Molecular‐dynamics computer simulation of an aqueous NaCl solution: Structure , 1992 .

[19]  Max L. Berkowitz,et al.  Computer simulation of a water/membrane interface , 1991 .

[20]  K V Damodaran,et al.  Structure and dynamics of the dilauroylphosphatidylethanolamine lipid bilayer. , 1992, Biochemistry.

[21]  Alfons Geiger,et al.  Molecular dynamics study of the hydration of Lennard‐Jones solutes , 1979 .

[22]  Bernard Pettitt,et al.  Peptides in ionic solutions: A comparison of the Ewald and switching function techniques , 1991 .

[23]  R. O. Watts,et al.  Monte Carlo studies of liquid water , 1974 .

[24]  Robert B. Gennis,et al.  Biomembranes: Molecular Structure and Function , 1988 .

[25]  J. Andrew McCammon,et al.  Computer Simulation and the Design of New Biological Molecules , 1986 .

[26]  Bo Jönsson,et al.  Molecular dynamics simulations of a sodium octanoate micelle in aqueous solution , 1986 .

[27]  M. Rao,et al.  Hydrophobic hydration around a pair of apolar species in water , 1979 .

[28]  J. Seelig,et al.  Hydration of Escherichia coli lipids. Deuterium T1 relaxation time studies of phosphatidylglycerol, phosphatidylethanolamine and phosphatidylcholine. , 1983, Biochimica et biophysica acta.

[29]  D. Engelman,et al.  Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. , 1983, Journal of molecular biology.

[30]  S. Marčelja,et al.  Repulsion of interfaces due to boundary water , 1976 .

[31]  R. Griffin,et al.  Deuterium NMR investigation of ether- and ester-linked phosphatidylcholine bilayers. , 1985, Biochemistry.

[32]  L. Verlet.  Computer "Experiments" on Classical Fluids. I. Thermodynamical Properties of Lennard-Jones Molecules , 1967 .

[33]  E. Guàrdia,et al.  Molecular dynamics simulation of single ions in aqueous solutions: effects of the flexibility of the water molecules , 1990 .

[34]  M. Rami Reddy,et al.  A molecular dynamics study of the structure and dynamics of water between dilauroylphosphatidylethanolamine bilayers , 1992 .

[35]  J Brickmann,et al.  Molecular dynamics studies of the interface between a model membrane and an aqueous solution. , 1991, Biophysical journal.

[36]  B. Brooks,et al.  The effects of truncating long‐range forces on protein dynamics , 1989, Proteins.

[37]  Terry R. Stouch,et al.  Computer simulation of a phospholipid monolayer‐water system: The influence of long range forces on water structure and dynamics , 1993 .

[38]  C R Worthington,et al.  X-ray diffraction evidence for the presence of discrete water layers on the surface of membranes. , 1991, Biochimica et biophysica acta.

[39]  A. Hagler,et al.  Theoretical studies of the structure and molecular dynamics of a peptide crystal. , 1988, Biochemistry.

[40]  H. Berendsen,et al.  Molecular dynamics simulation of a smectic liquid crystal with atomic detail , 1988 .

[41]  S H White,et al.  Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. I. Scaling of neutron data and the distributions of double bonds and water. , 1991, Biophysical journal.

[42]  P. Rossky,et al.  The equilibrium solvation structure for the solvent‐separated hydrophobic bond , 1985 .

[43]  Othmar Steinhauser,et al.  Reaction field simulation of water , 1982 .

[44]  Bruce J. Berne,et al.  A Monte Carlo study of structural and thermodynamic properties of water: dependence on the system size and on the boundary conditions , 1980 .

[45]  D. Small,et al.  Phase equilibria and structure of dry and hydrated egg lecithin. , 1967, Journal of lipid research.

[46]  R. Pearson,et al.  The molecular structure of lecithin dihydrate , 1979, Nature.

[47]  Hans Binder,et al.  Behaviour of water at membrane surfaces - a molecular dynamics study , 1985 .

[48]  F. Stillinger,et al.  Improved simulation of liquid water by molecular dynamics , 1974 .

[49]  V A Parsegian,et al.  Membrane dipole potentials, hydration forces, and the ordering of water at membrane surfaces. , 1992, Biophysical journal.

[50]  Maria Luisa Foresti,et al.  A Monte Carlo simulation of water molecules near a charged wall , 1989 .

[51]  H. Schreiber,et al.  Molecular dynamics studies of solvated polypeptides: Why the cut-off scheme does not work , 1992 .

[52]  Ronald M. Levy,et al.  Computer simulations of the dielectric properties of water: Studies of the simple point charge and transferrable intermolecular potential models , 1989 .