Time-dependent fluorescence shift (TDFS) of Laurdan embedded in phospholipid bilayers reports on hydration and mobility of the phospholipid acylgroups. Exchange of H2O with D2O prolongs the lifetime of lipid-water and lipid-water-lipid interactions, which is reflected in a significantly slower TDFS kinetics. Combining TDFS measurements in H2O and D2O hydrated bilayers with atomistic molecular dynamics (MD) simulations provides a unique tool for characterization of the hydrogen bonding at the acylgroup level of lipid bilayers. In this work, we use this approach to study the influence of fluoride anions on the properties of cationic bilayers composed of trimethylammonium-propane (DOTAP). The results obtained for DOTAP are confronted with those for neutral phosphatidylcholine (DOPC) bilayers. Both in DOTAP and DOPC H2O/D2O exchange prolongs hydrogen-bonding lifetime and does not disturb bilayer structure. These results are confirmed by MD simulations. TDFS experiments show, however, that for DOTAP this effect is cancelled in the presence of fluoride ions. We interpret these results as evidence that strongly hydrated fluoride is able to steal water molecules that bridge lipid carbonyls. Consequently, when attracted to DOTAP bilayer, fluoride disrupts the local hydrogen-bonding network, and the differences in TDFS kinetics between H2O and D2O hydrated bilayers are no longer observed. A distinct behavior of fluoride is also evidenced by MD simulations, which show different lipid-ion binding for Cl and F.

1.
G.
Nemethy
and
H. A.
Scheraga
,
J. Chem. Phys.
41
,
680
(
1964
).
2.
C. S.
Pittendrigh
,
P. C.
Caldarola
, and
E. S.
Cosbey
,
Proc. Natl. Acad. Sci. U.S.A.
70
,
2037
(
1973
).
3.
V. G.
Bruce
and
C. S.
Pittendrigh
,
J. Cell. Comp. Physiol.
56
,
25
(
1960
).
4.
D. J.
Kushner
,
A.
Baker
, and
T. G.
Dunstall
,
Can. J. Physiol. Pharmacol.
77
,
79
(
1999
).
5.
W. H.
Adams
and
D. G.
Adams
,
J. Pharmacol. Exp. Ther.
244
,
633
(
1988
).
6.
J.
Lamprecht
,
D.
Schroeter
, and
N.
Paweletz
,
J. Cell Sci.
98
,
463
(
1991
).
7.
8.
K. B.
Wiberg
,
Chem. Rev.
55
,
713
(
1955
).
9.
L.
Benjamin
and
G. C.
Benson
,
J. Phys. Chem.
67
,
858
(
1963
).
10.
S.
Scheiner
and
M.
Cuma
,
J. Am. Chem. Soc.
118
,
1511
(
1996
).
11.
P.
Cioni
and
G. B.
Strambini
,
Biophys. J.
82
,
3246
(
2002
).
12.
G. C.
Kresheck
,
H.
Schneider
, and
H. A.
Scheraga
,
J. Phys. Chem.
69
,
3132
(
1965
).
13.
M. J.
Parker
and
A. R.
Clarke
,
Biochemistry
36
,
5786
(
1997
).
14.
P.
Sasisanker
,
A.
Oleinikova
,
H.
Weingartner
,
R.
Ravindra
, and
R.
Winter
,
Phys. Chem. Chem. Phys.
6
,
1899
(
2004
).
15.
P. R.
Andjus
,
A. A.
Kataev
,
A. A.
Alexandrov
,
D.
Vucelić
, and
G. N.
Berestovsky
,
J. Membr. Biol.
142
,
43
(
1994
).
16.
P. R.
Andjus
and
D.
Vucelic
,
J. Membr. Biol.
115
,
123
(
1990
).
17.
C.
Elsing
,
A.
Hirlinger
,
E. L.
Renner
,
B. H.
Lauterburg
,
P. J.
Meier
, and
J.
Reichen
,
Biochem. J.
307
(
Pt 1
),
175
(
1995
).
18.
B.
Prod'hom
,
D.
Pietrobon
, and
P.
Hess
,
Nature
329
,
243
(
1987
).
19.
S.
Vasdev
,
I. P.
Gupta
,
C. A.
Sampson
,
L.
Longerich
, and
S.
Parai
,
Can. J. Cardiol.
9
,
802
(
1993
).
20.
S.
Vasdev
,
V. M.
Prabhakaran
,
M.
Whelan
,
C. A.
Ford
,
L.
Longerich
, and
S.
Parai
,
Artery
21
,
124
(
1994
).
21.
J.
Grdadolnik
,
J.
Kidrič
, and
D.
Hadži
,
Chem. Phys. Lipids
59
,
57
(
1991
).
22.
M.
Pasenkiewicz-Gierula
,
Y.
Takaoka
,
H.
Miyagawa
,
K.
Kitamura
, and
A.
Kusumi
,
J. Phys. Chem. A
101
,
3677
(
1997
).
23.
V. V.
Volkov
,
Y.
Takaoka
, and
R.
Righini
,
J. Phys. Chem. B
113
,
4119
(
2009
).
24.
C. H.
Chen
,
J. Phys. Chem.
86
,
3559
(
1982
).
25.
G.
Lipka
,
B. Z.
Chowdhry
, and
J. M.
Sturtevant
,
J. Phys. Chem.
88
,
5401
(
1984
).
26.
L. D.
Ma
,
R. L.
Magin
,
G.
Bacic
, and
F.
Dunn
,
Biochim. Biophys. Acta
978
,
283
(
1989
).
27.
H.
Matsuki
,
H.
Okuno
,
F.
Sakano
,
M.
Kusube
, and
S.
Kaneshina
,
Biochim. Biophys. Acta
1712
,
92
(
2005
).
28.
J.
Milhaud
,
E.
Hantz
, and
J.
Liquier
,
Langmuir
22
,
6068
(
2006
).
29.
K.
Ohki
,
Biochem. Biophys. Res. Commun.
174
,
102
(
1991
).
30.
T.
Róg
,
K.
Murzyn
,
J.
Milhaud
,
M.
Karttunen
, and
M.
Pasenkiewicz-Gierula
,
J. Phys. Chem. B
113
,
2378
(
2009
).
31.
L.
Beranová
,
J.
Humpolíčková
,
J.
Sýkora
,
A.
Benda
,
L.
Cwiklik
,
P.
Jurkiewicz
,
G.
Gröbner
, and
M.
Hof
,
Phys. Chem. Chem. Phys.
14
,
14516
(
2012
).
32.
H. J.
Bakker
,
Chem. Rev.
108
,
1456
(
2008
).
33.
F.
Hofmeister
,
Arch. Exp. Pathol. Pharmakol.
25
,
1
(
1888
).
34.
W.
Kunz
,
J.
Henle
, and
B. W.
Ninham
,
Curr. Opin. Colloid Interface Sci.
9
,
19
(
2004
).
35.
J. J.
Garcia-Celma
,
L.
Hatahet
,
W.
Kunz
, and
K.
Fendler
,
Langmuir
23
,
10074
(
2007
).
36.
A. A.
Gurtovenko
,
M.
Miettinen
,
M.
Karttunen
, and
I.
Vattulainen
,
The J. Phys. Chem. B
109
,
21126
(
2005
).
37.
P. M.
Macdonald
and
J.
Seelig
,
Biochemistry
27
,
6769
(
1988
).
38.
P.
Jurkiewicz
,
L.
Cwiklik
,
A.
Vojtíšková
,
P.
Jungwirth
, and
M.
Hof
,
Biochim. Biophys. Acta
1818
,
609
(
2012
).
39.
S.
Pokorna
,
P.
Jurkiewicz
,
L.
Cwiklik
,
M.
Vazdar
, and
M.
Hof
,
Faraday Discuss.
160
,
341
(
2013
).
40.
M. L.
Horng
,
J. A.
Gardecki
,
A.
Papazyan
, and
M.
Maroncelli
,
J. Phys. Chem.
99
,
17311
(
1995
).
41.
R.
Richert
,
F.
Stickel
,
R. S.
Fee
, and
M.
Maroncelli
,
Chem. Phys. Lett.
229
,
302
(
1994
).
42.
P.
Jurkiewicz
,
J.
Sýkora
,
A.
Olzyńska
,
J.
Humpolícková
, and
M.
Hof
,
J. Fluoresc.
15
,
883
(
2005
).
43.
A. P.
Demchenko
,
Y.
Mely
,
G.
Duportail
, and
A. S.
Klymchenko
,
Biophys. J.
96
,
3461
(
2009
).
44.
L. A.
Bagatolli
,
Fluorescent Methods to Study Biological Membranes
(
Springer
,
Berlin, Heidelberg
,
2013
), Vol.
13
, p.
3
.
45.
J.
Sykora
,
P.
Kapusta
,
V.
Fidler
, and
M.
Hof
,
Langmuir
18
,
571
(
2002
).
46.
J.
Barucha-Kraszewska
,
S.
Kraszewski
,
P.
Jurkiewicz
,
C.
Ramseyer
, and
M.
Hof
,
Biochim. Biophys. Acta
1798
,
1724
(
2010
).
47.
P. O.
Westlund
,
J. Phys. Chem. B
104
,
6059
(
2000
).
48.
B.
Halle
and
L.
Nilsson
,
J. Phys. Chem. B
113
,
8210
(
2009
).
49.
P.
Jurkiewicz
,
L.
Cwiklik
,
P.
Jungwirth
, and
M.
Hof
,
Biochimie
94
,
26
(
2012
).
50.
O.
Berger
,
O.
Edholm
, and
F.
Jahnig
,
Biophys. J.
72
,
2002
(
1997
).
51.
H. J. C.
Berendsen
,
J. P. M.
Postma
,
W. F.
Van Gunsteren
, and
J.
Hermans
, in
Intermolecular Forces
(
D. Reidel Publishing Company
,
Dordrecht
,
1981
), p.
331
.
52.
B.
Hess
,
C.
Kutzner
,
D.
van der Spoel
, and
E.
Lindahl
,
J. Chem. Theory Comput.
4
,
435
(
2008
).
53.
D.
Horinek
,
S. I.
Mamatkulov
, and
R. R.
Netz
,
J. Chem. Phys.
130
,
124507
(
2009
).
54.
U.
Essmann
,
L.
Perera
,
M. L.
Berkowitz
,
T.
Darden
,
H.
Lee
, and
L. G.
Pedersen
,
J. Chem. Phys.
103
,
8577
(
1995
).
55.
M.
Parrinello
and
A.
Rahman
,
J. Appl. Phys.
52
,
7182
(
1981
).
57.
B.
Hess
,
H.
Bekker
,
H. J. C.
Berendsen
, and
J. G. E. M.
Fraaije
,
J. Comput. Chem.
18
,
1463
(
1997
).
58.
R. W.
Hockney
,
S. P.
Goel
, and
J. W.
Eastwood
,
J. Comput. Phys.
14
,
148
(
1974
).
59.
R.
Macháň
,
P.
Jurkiewicz
,
A.
Olżyńska
,
M.
Olšinová
,
M.
Cebecauer
,
A.
Marquette
,
B.
Bechinger
, and
M.
Hof
,
Langmuir
30
,
6171
6179
(
2014
);
[PubMed]
G.
Först
,
L.
Cwiklik
,
P.
Jurkiewicz
,
R.
Schubert
, and
M.
Hof
,
Eur. J. Pharm. Biopharm.
87
,
559
569
;
[PubMed]
see also Ref. 39.
60.
M.
Sajadi
,
M.
Weinberger
,
H. A.
Wagenknecht
, and
N. P.
Ernsting
,
Phys. Chem. Chem. Phys.
13
,
17768
(
2011
).
61.
E.
Leontidis
and
A.
Aroti
,
J. Phys. Chem. B
113
,
1460
(
2009
).
62.
R.
Vacha
,
P.
Jurkiewicz
,
M.
Petrov
,
M. L.
Berkowitz
,
R. A.
Bockmann
,
J.
Barucha-Kraszewska
,
M.
Hof
, and
P.
Jungwirth
,
J. Phys. Chem. B
114
,
9504
(
2010
).
63.
Y.
Kawashima
,
K.
Suzuki
, and
M.
Tachikawa
,
J. Phys. Chem. A
117
,
5205
(
2013
).
64.
K.
Suzuki
,
M.
Tachikawa
, and
M.
Shiga
,
J. Chem. Phys.
132
,
144108
(
2010
).
65.
P.
Jurkiewicz
,
A.
Olzynska
,
M.
Langner
, and
M.
Hof
,
Langmuir
22
,
8741
(
2006
).
You do not currently have access to this content.