The atomic-scale hydration structure around the 1,2-dioleoyl-sn-glycero-3-phosphoethanolamine (DOPE) headgroup in a chloroform/water solution has been investigated using neutron diffraction enhanced by isotopic substitution and NMR, coupled with empirical potential structure refinement and molecular dynamics simulations. The results obtained show the preferential binding sites for water molecules on the DOPE headgroups, with the most predominant interactions being with the ammonium and phosphate groups. Interestingly, the level of hydration, as well as the association of DOPE molecules, varies according to the simulation method used. The results here suggest the presence of a tight water network around these lipid headgroups that could affect the permeability of the membrane for lipid-mediated diffusion.
REFERENCES
1.
A.
van Dalen
and B.
de Kruijff
, “The role of lipids in membrane insertion and translocation of bacterial proteins
,” Biochim. Biophys. Acta
1694
, 97
–109
(2004
), protein export/secretion in bacteria.2.
S.
Suetsugu
, S.
Kurisu
, and T.
Takenawa
, “Dynamic shaping of cellular membranes by phospholipids and membrane-deforming proteins
,” Physiol. Rev.
94
, 1219
–1248
(2014
).3.
J. E.
Vance
and G.
Tasseva
, “Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells
,” Biochim. Biophys. Acta
1831
, 543
–554
(2013
).4.
D. E.
Vance
, “Phospholipid methylation in mammals: From biochemistry to physiological function
,” Biochim. Biophys. Acta
1838
, 1477
–1487
(2014
).5.
D. A.
Pink
, S.
McNeila
, B.
Quinna
, and M. J.
Zuckermann
, “A model of hydrogen bond formation in phosphatidylethanolamine bilayers
,” Biochim. Biophys. Acta
1368
, 289
–305
(1998
).6.
R. M.
Venable
, F. L. H.
Brown
, and R. W.
Pastor
, “Mechanical properties of lipid bilayers from molecular dynamics simulation
,” Chem. Phys. Lipids
192
, 60
–74
(2015
).7.
J. L.
Mikitsh
and A.-M.
Chacko
, “Pathways for small molecule delivery to the central nervous system across the blood-brain barrier
,” Perspect. Med. Chem.
6
, 11
–24
(2014
).8.
W. A.
Banks
, “Characteristics of compounds that cross the blood-brain barrier
,” BMC Neurol.
9
, S1
–S3
(2009
).9.
C. W.
Gibby
and J.
Hall
, “XCIV—The system water-chloroform
,” J. Chem. Soc.
1931
, 691
–693
.10.
R. J.
Gillams
, J. V.
Busto
, S.
Busch
, F. M.
Goñi
, C. D.
Lorenz
, and S. E.
McLain
, “Solvation and hydration of the ceramide headgroup in a non-polar solution
,” J. Phys. Chem. B
119
, 128
–139
(2015
).11.
R. J.
Gillams
, C. D.
Lorenz
, and S. E.
McLain
, “Comparative atomic-scale hydration of the ceramide and phosphocholine headgroup in solution and bilayer environments
,” J. Chem. Phys.
144
, 225101
(2016
).12.
F.
Foglia
, M. J.
Lawrence
, C. D.
Lorenz
, and S. E.
McLain
, “On the hydration of the phosphocholine headgroup in aqueous solution
,” J. Chem. Phys.
133
, 145103
(2010
).13.
A. P.
Dabkowska
, F.
Foglia
, M. J.
Lawrence
, C. D.
Lorenz
, and S. E.
McLain
, “On the solvation structure of dimethylsulfoxide/water around the phosphatidylcholine head group in solution
,” J. Chem. Phys.
135
, 225105
(2011
).14.
N. H.
Rhys
, M. A.
Al-Badri
, R. M.
Ziolek
, R. J.
Gillams
, L. E.
Collins
, M.
Lawrence
, C. D.
Lorenz
, and S. E.
McLain
, “On the solvation of the phosphocholine headgroup in an aqueous propylene glycol solution
,” J. Chem. Phys.
48
, 135102
(2018
).15.
H. E.
Gottlieb
, V.
Kotlyar
, and A.
Nudelman
, “NMR chemical shifts of common laboratory solvents as trace impurities
,” J. Organic Chem.
62
, 7512
–7515
(1997
).16.
A. K.
Soper
, “GudrunN and GudrunX: Programs for correcting raw neutron and X-ray diffraction data to differential scattering cross section
,” RAL Report No. RAL-TR-201, 2011
.17.
V. F.
Sears
, “Neutron scattering lengths and cross sections
,” Neutron News
3
, 26
–37
(1992
).18.
S. E.
McLain
, C. J.
Benmore
, J. E.
Siewenie
, J.
Urquidi
, and J. F. C.
Turner
, “On the structure on hydrogen fluoride
,” Angew. Chem., Int. Ed.
43
, 1952
–1955
(2004
).19.
A. K.
Soper
, “Partial structure factors from disordered materials diffraction data: An approach using empirical potential structure refinement
,” Phys. Rev. B
72
, 104204
–104215
(2005
).20.
A. K.
Soper
, “Empirical potential Monte Carlo simulation of fluid structure
,” Chem. Phys.
202
, 295
–306
(1996
).21.
A. J.
Johnston
, S.
Busch
, L. C.
Pardo
, S. K.
Callear
, P. C.
Biggin
, and S. E.
McLain
, “On the atomic structure of cocaine in solution
,” Phys. Chem. Chem. Phys.
18
, 991
–999
(2016
).22.
J. J.
Shephard
, S. K.
Callear
, S.
Imberti
, J. S. O.
Evans
, and C. G.
Salzmann
, “Microstructures of negative and positive azeotropes
,” Phys. Chem. Chem. Phys.
18
, 19227
–19235
(2016
).23.
N.
Steinke
, R. J.
Gillams
, L. C.
Pardo
, C. D.
Lorenz
, and S. E.
McLain
, “Atomic scale insights into urea-peptide interactions in solution
,” Phys. Chem. Chem. Phys.
18
, 3862
–3870
(2016
).24.
N.
Steinke
, A.
Genina
, C. D.
Lorenz
, and S. E.
McLain
, “Salt interactions in solution prevent direct association of urea with a peptide backbone
,” J. Phys. Chem. B
121
, 1866
–1876
(2017
).25.
N. H.
Rhys
, R. J.
Gillams
, L. E.
Collins
, S. K.
Callear
, M. J.
Lawrence
, and S. E.
McLain
, “On the structure of an aqueous propylene glycol solution
,” J. Chem. Phys.
145
, 224504
(2016
).26.
A.
Silva-Santisteban
, N.
Steinke
, A. J.
Johnston
, G. N.
Ruiz
, L.
Carlos Pardo
, and S. E.
McLain
, “On the structure of prilocaine in aqueous and amphiphilic solutions
,” Phys. Chem. Chem. Phys.
19
, 12665
–12673
(2017
).27.
N. H.
Rhys
, F.
Bruni
, S.
Imberti
, S. E.
McLain
, and M. A.
Ricci
, “Glucose and mannose: A link between hydration and sweetness
,” J. Phys. Chem. B
121
, 7771
–7776
(2017
).28.
M.
Gilmore
, L. M.
Moura
, A. H.
Turner
, M.
Swadzba-Kwasny
, S. K.
Callear
, J. A.
McCune
, O. A.
Scherman
, and J. D.
Holbrey
, “A comparison of choline:urea and choline:oxalic acid deep eutectic solvents at 338 K
,” J. Chem. Phys.
148
, 193823
(2018
).29.
A. H.
Turner
, S.
Imberti
, M.
Swadzba-Kwasny
, and J. D.
Holbrey
, “Applying neutron diffraction with isotopic substitution to the structure and proton-transport pathways in protic imidazolium bis(trifluoromethyl)sulfonylimide ionic liquids
,” Faraday Disc.
206
, 247
–263
(2018
).30.
O. S.
Hammond
, D. T.
Bowron
, and K. J.
Edler
, “The effect of water upon deep eutectic solvent nanostructure: An unusual transition from ionic mixture to aqueous solution
,” Angew. Chem., Int. Ed.
129
, 9914
–9917
(2017
).31.
S.
Lenton
, N. H.
Rhys
, J. J.
Towey
, A. K.
Soper
, and L.
Dougan
, “Highly compressed water structure observed in a perchlorate aqueous solution
,” Nat. Commun.
8
, 919
(2017
).32.
J. B.
Klauda
, R. M.
Venable
, J. A.
Freites
, J. W.
O’Connor
, D. J.
Tobias
, C.
Mondragon-Ramirez
, I.
Vorobyov
, A. D.
MacKerell
, Jr., and R. W.
Pastor
, J. Phys. Chem. B
114
, 7830
–7843
(2010
).33.
S.
Jo
, T.
Kim
, V. G.
Iyer
, and W.
Im
, “CHARMM-GUI: A web-based graphical user interface for CHARMM
,” J. Comput. Chem.
29
, 1859
–1865
(2008
).34.
E. L.
Wu
, X.
Cheng
, S.
Jo
, H.
Rui
, K. C.
Song
, E. M.
Dávila-Contreras
, Y.
Qi
, J.
Lee
, V.
Monje-Galvan
, R. M.
Venable
, J. B.
Klauda
, and W.
Im
, “CHARMM-GUI membrane builder toward realistic biological membrane simulations
,” J. Comput. Chem.
35
, 1997
–2004
(2014
).35.
H. J. C.
Berendsen
, J. R.
Grigera
, and T. P.
Straatsma
, “The missing term in effective pair potentials
,” J. Phys. Chem.
91
, 6269
–6271
(1987
).36.
W. L.
Jorgensen
, D. S.
Maxwell
, and J.
Tirado-Rives
, “Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids
,” J. Am. Chem. Soc.
118
, 11225
–11236
(1996
).37.
W. L.
Jorgensen
, J.
Chandrasekhar
, J. D.
Madura
, R. W.
Impey
, and M. L.
Klein
, “Comparison of simple potential functions for simulating liquid water
,” J. Chem. Phys.
79
, 926
–935
(1983
).38.
W. E.
Reiher
, “Theoretical studies of hydrogen bonding
,” Ph.D. thesis, Harvard University
, 1985
.39.
C.
Caleman
, P. J.
van Maaren
, M.
Hong
, J. S.
Hub
, L. T.
Costa
, and D.
van der Spoel
, “Force field benchmark of organic liquids: Density, enthalpy of vaporization, heat capacities, surface tension, isothermal compressibility, volumetric expansion coefficient, and dielectric constant
,” J. Chem. Theory Comput.
8
, 61
–74
(2012
).40.
J.-P.
Ryckaert
, G.
Ciccotti
, and H. J.
Berendsen
, “Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes
,” J. Comput. Phys.
23
, 327
–341
(1977
).41.
S.
Plimpton
, “Fast parallel algorithms for short-range molecular dynamics
,” J. Comput. Phys.
117
, 1
–19
(1995
).42.
R. W.
Hockney
and J. W.
Eastwood
, Computer Simulation Using Particles
(Adam Hilger
, New York
, 1988
).43.
R. J.
Gillams
, C. D.
Lorenz
, and S. E.
McLain
, “On the hydration and conformation of cocaine in solution
,” Chem. Phys. Lett.
676
, 58
–64
(2017
).44.
A. A.
Hagberg
, D. A.
Schult
, and P.
Swart
, “Exploring network structure, dynamics, and function using NetworkX
,” in Proceedings of the 7th Python in Science Conference (SciPy2008)
, edited by G.
Varoquaux
, T.
Vaught
, and J.
Millman
(SciPy
, Pasadena, CA, USA
, 2008
), pp. 11
–15
.45.
P. M.
Smith
, R. M.
Ziolek
, E.
Gazzarini
, D. M.
Owen
, and C. D.
Lorenz
, “On the interaction of hyaluronic acid with synovial fluid lipid membranes
,” Phys. Chem. Chem. Phys.
(submitted).46.
See https://gcm.upc.edu/en/members/luis-carlos/angula/angula for ANGULA software.
47.
S.
Busch
, C. D.
Lorenz
, J.
Taylor
, L. C.
Pardo
, and S. E.
McLain
, “Short-range interactions of concentrated proline in aqueous solution
,” J. Phys. Chem. B
118
, 14267
–14277
(2014
).48.
A. J.
Sodt
and R. W.
Pastor
, “Bending free energy from simulation: Correspondence of planar and inverse hexagonal lipid phases
,” Biophys. J.
104
, 2202
–2211
(2013
).49.
A. J.
Sodt
and R. W.
Pastor
, “Molecular modelling of lipid membrane curvature induction by a peptide: More than simply shape
,” Biophys. J.
106
, 1958
–1969
(2014
).50.
A. K.
Soper
, “The excluded volume effect in confined fluids and liquid mixtures
,” J. Phys.: Condens. Matter
9
, 2399
(1997
).51.
J. C.
Mathai
, S.
Tristam-Nagle
, J. F.
Nagle
, and M. L.
Zeidel
, “Structural determinants of water permeability through the lipid membrane
,” J. Gen. Physiol.
131
, 69
–76
(2008
).52.
J. F.
Nagle
, J. C.
Mathai
, M. L.
Zeidel
, and S.
Tristam-Nagle
, “Theory of passive permeability through lipid bilayers
,” J. Gen. Physiol.
131
, 77
–85
(2008
).© 2019 Author(s).
2019
Author(s)
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