The Interfacial Tension of the Lipid Membrane Formed
from Lipid–Amino Acid Systems
Aneta D. Petelska•Monika Naumowicz•
Zbigniew A. Figaszewski
Published online: 13 May 2011
? The Author(s) 2011. This article is published with open access at Springerlink.com
posed of phosphatidylcholine (lecithin, PC)–valine (Val),
phosphatidylcholine–isoleucine (Ile), phosphatidylcholine–
has been studied. The membrane components formed 1:1
complexes. The interfacial tension measurements were used
to determine the membrane surface concentration A3
membrane interfacial tension c3, and the stability constant K.
The interfacial tension of lipid membranes com-
Phosphatidylcholine ? Valine ? Isoleucine ? Tyrosine ?
Phenylalanine ? Complex 1:1
Interfacial tension ? Bilayer membrane ?
Natural cell membranes have been studied by numerous
techniques including physicochemical ones. An important
property of a cell membrane is its interfacial tension, which
determines its rigidity and, as a result, affects its stability.
A cell membrane is a very complex system, and it contains
various structural components that can influence its inter-
facial tension. Therefore, it is easier to study the effect of
various factors; e.g., amino acid–lipid interaction using
artificial phospholipid bilayer model membranes. The
properties of the artificial membrane should be well known
and generally similar to the properties of the membranes of
living cells. Lipid monolayers, lipid bilayers, collodion,
cellophane, millipore, ion-exchanger, or other membranes
have been used as artificial membranes , but the inter-
facial tension of a cell membrane is best measured by
means of a spherical bilayer lipid model membrane.
Therefore, although they are usually only present in low
concentrations in cells, amino acids represent interesting
model substances to examination the interaction between
amino acids and bilayer lipid membranes. These interactions
have been examined used numerous experimental studies
in a lipid bilayer of small molecules mimicking 17 natural
amino acids in atomistic detail by molecular dynamics sim-
of the preferred location and orientation of each side chain as
well as the preferred charge state for ionizable residues.
To understand complex biological systems it is valuable
to analyze simpler model systems. It would be useful, for
example, to be able to determine the influence of individual
amino acids on the interactions of peptides with a cell
membrane. Jacobs and White used a variety of techniques
to examine the thermodynamics and binding of a general
class of tripeptides, to small phosphatidylcholine vesicles
. These experiments revealed peptide induced alterations
of the lipid order and modulations of the lipid acyl chain
motion. Later work related these thermodynamic parame-
ters with structural information from neutron diffraction
experiments . These experiments were used to deter-
mine the general location of the peptide in the bilayer, if
the peptide inserted in hydrocarbon region or was confined
to the water–hydrocarbon interface. Specific information
concerning the structure of the lipid–peptide complex
A. D. Petelska (&) ? M. Naumowicz ? Z. A. Figaszewski
Institute of Chemistry, University in Bialystok, Al.
J. Pilsudskiego 11/4, 15-443 Bialystok, Poland
e-mail: firstname.lastname@example.org; email@example.com
Z. A. Figaszewski
Laboratory of Electrochemical Power Sources, Faculty of
Chemistry, University of Warsaw, Pasteur St. 1, 02-093 Warsaw,
Cell Biochem Biophys (2011) 61:289–296
would be extremely useful in further understanding the role
of individual amino acids in peptide–lipid interactions.
It is well known the importance of investigations of inter-
actions between proteins and biological membranes. We
decided to give a deeper sight to this problem by the determi-
of proteins and membranes: amino acid molecules and
phospholipid bilayers correspondingly, using interfacial ten-
sion method. By means of interfacial tension method,
bilayer behavior influence on the peptide–lipid interaction.
The effects of membrane composition on interfacial
tension were previously described in phosphatidylcholine–
other lipid , phosphatidylcholine–fatty acid, and
phosphatidylcholine–amine systems . This work is a
continuation of our studies concerning the interaction of
lipid bilayers with molecules of increasing complexity
using membranes composed of phosphatidylcholine–amino
acid system. We describe the dependence of interfacial
tension on membrane composition in phosphatidylcholine
(PC)–valine (Val), PC–isoleucine (Ile), PC–tyrosine (Tyr),
and PC–phenylalanine (Phe) over a possible range of
compositions, and present a comparison of the stability
constants of the complexes and the surface areas occupied
by the membrane components.
In the cases where the membrane components do not form
chemical compounds, their interaction can be described by
the following set of equations [13, 14]:
c1m1A1þ c2m2A2¼ c
x1þ x2¼ 1
components 1 and 2; m1;m2(mol m-2) are the quantities of
components 1 and 2 per unit area of the membrane; c1;c2
(N m-1) are the interfacial tensions of membranes assem-
bled from pure components 1 and 2; c (N m-1) is the
measured interfacial tension of the membrane; and x1;x2
are the solution mole fractions of components 1 and 2.
The elimination of m1and m2yields the linear equation:
(mol m-2) are the surface concentration of
c ? c1
capable of forming a complex. The stoichiometry of the
complex may vary, but because the first stability constant in
these complexes is usually the largest , we assumed that
the complexes are primarily of 1:1 stoichiometry.
In cases where the membrane components form a 1:1
complex, interactions in the membrane may be described
by a previously published set of equations .
The equilibrium between the individual components and
the complex is represented by:
AðComponent1Þ þ BðComponent2Þ , ABðComplex)
and the basic equation describing the interaction between
components 1 and 2 can be written as [11, 14]:
c ? c1
þ c3? c2
þ c3? c
where B1¼ A3=A1and B2¼ A3=A2:
Equation 3 may be simplified by taking into account the
high stability constant of the complex. Applying this sim-
plification results in linear behavior for small (x2\x1) and
large (x2[x1) x2values [11, 14].
ðÞB2x1þ c ? c2
ÞB1x2þ c1? c2
3B1B2 c ? c1
ÞB1x2? c ? c2
½? c3? c1
Þ x1? x2
Þ x2? x1
Þ x1? x2
ðððÞ þ c3? c
¼ ?B1c3þ B1c
ð ¼ ?B2c3þ B2c
When calculating the stability constant for the complex,
Eq. 3 can be simplified to x1¼ x2.
???1c ? c3
2? c A?1
2? c A?1
The parameters describing the complex may be used to
calculate theoretical points using the equation presented
below (agreement between the theoretical and experimental
values implies that the system is well described by the
ðÞ a3? a1
Þ a1þ a2
Þ a3? a1
Þ ? a4A?1
ðð Þ þ a4A?1
ðÞ ¼ 0
þ c2? c3
ðÞ x2? x1
ð Þ þ c1? c3
290 Cell Biochem Biophys (2011) 61:289–296
For systems containing two lipid components, 1:1
complex formation was assumed to be the explanation for
deviation from the additivity rule. Model curves were
constructed usingcalculated parameters such as equilibrium
constants, molecular areas of the complexes, and interfacial
tension of molecules and complexes. The accuracy of the
models was verified by comparison to experimental results.
Measuring Apparatus and Measuring Procedures
The interfacial tension method is based on Young and
2c ¼ RDp:
The interfacial tension, c, in a lipid bilayer sample is
determined by measuring the radius of curvature of the
convex surface, R, formed when a pressure difference, Dp
is applied across the bilayer .
The apparatus and measurement method were described
in previous papers [13, 17]. The measurement vessel con-
sists of two glass chambers separated by a mount holding a
1.5 mm diameter circular Teflon element axially pierced
by a small orifice. Spherical membranes were formed by
the Mueller–Rudin method  on the flat end of the
Teflon element. Both chambers were filled with an elec-
trolyte solution. The membrane-forming solution was
introduced to the flat wall of the Teflon element using a
micropipette, and pressure was applied to the left chamber
using a manometer (VEB).
The convexity of the spherical cap was measured by
means of a microscope with an objective equipped with a
scale with 0.1-mm-interval scale marks. Therefore, the
instrument readings of the lipid spherical cap were made
with 0.05 mm precision. The convexity of the lipid mem-
brane of the spherical cap, together with the Teflon element
diameter corresponding to the lipid spherical cap diameter,
yielded the radius of curvature. The measurement of the
spherical cap was difficult because the spherical cap is
hardly visible. While using yellow light its visibility gets
The radius of curvature, R, was determined using this
value and the diameter of the Teflon element, corre-
sponding to the diameter of the lipid cap and the convexity
of the lipid membrane, which was presented below in
drawing a and b:
where R radius of curvature, r radius of the Teflon cap,
h convexity of the lipid membrane.
Radius of curvature was calculated from equation:
R ¼ r2þ h2?2h:
membrane and overpressure provoking the membrane
convexity. Then we calculated the interfacial tension val-
ues from radius of curvature and pressure difference values
according to Young and Laplace’s equation.
The interfacial tension was measured on a freshly cre-
ated lipid bilayer membrane 12–15 times. For each mem-
brane about 10 instrument readings of the lipid spherical
cap diameter, formed by pressure difference applied on
both sides, were made. These measurements were made
within the whole range, from the very low values of
the lipid spherical cap diameter to those almost equal to the
Teflon element radius. From all of instrument readings the
arithmetic mean and standard deviation were enumerated.
Measurements with preparation of the electrolyte solution
were made 2–3 times in order to test the repeatability of
these determinations. The experimental results are pre-
sented with error bars in the figures.
We measured radius of curvature of bilayer lipid
The following reagents were used for the preparation of the
1.Phosphatidylcholine (99%, Fluka) (fatty acid compo-
sition: 16:0 *33%, 18:0 *4%, 18:1 *30%, 18:2
*14%, 20:4 *4%).
Cell Biochem Biophys (2011) 61:289–296291
L-Valine (99.5%, Fluka);
L-Isoleucine (99.5%, Fluka);
L-Tyrosine (99.5%, Fluka);
Phenylalanine (99.5%, Fluka).
The molecular weights of the lecithin, valine, isoleucine,
tyrosine, and phenylalanine were approximately 752.08,
117.15, 131.17, 181.19, and 165.19 g mol-1, respectively.
The as-received phosphatidylcholine was purified by
dissolving in chloroform and evaporating the solvent under
argon. The stock membrane-forming solutions consisted of
20 mg cm-3of the desired substances (PC, Val, Ile, Tyr, or
Phe) in 20:1 n-decane:butanol. The solution containing the
membrane components was not saturated and could
therefore contain the components in any proportion. During
membrane formation, the solvent was removed, leaving a
membrane composed of lipids in the same ratio as the stock
solution. Bilayer membranes were obtained as bubbles at
the Teflon cap constituting a measuring vessel component.
The use of n-decane as the solvent allows one to obtain
membranes of thickness and capacity values similar to
those of membranes formed of monolayers [19, 20]; there
is almost no solvent retained in the bilayer. A small
quantity of butanol added has a negligible effect on the
interface tension values of the bilayers created; however, it
considerably accelerates the formation of the membranes.
The formation of the bilayers was monitored visually and
electrically by measuring the membrane capacitance at low
frequency (1 Hz). Capacity of the membranes increased
with time after bilayers formation until a steady-state value
was reached some 10–20 min later. The measurements
were begun only after the low frequency capacitance was
stable, increasing by, 1%/h. When the capacitance had
stabilized, it was assumed that diffusion of solvent out of
the bilayer was complete, although some n-decane mole-
cules would remain dissolved in the membrane interior.
The bilayers area was determined with a microscope with a
micrometer scale built into the lens.
The electrolyte solution contained 0.1 M potassium
chloride and was prepared using triple-distilled water and
KCl produced by POCh (Poland). The KCl was calcined to
remove any organic impurities.
All solvents were chromatographic standard grade. The
n-decane was purchased from Merck and the chloroform
and butanol were obtained from Aldrich.
All experiments were carried out at 293 ± 2 K.
Results and Discussion
The effect of the presence of amino acids on interfacial
tension of the membranes formed from PC was stud-
ied. The dependence of interfacial tension of the lipid
membrane as a function of composition was studied at
room temperature (293 ± 2 K) in all the feasible concen-
tration range. The interfacial tension values reported in this
paper refer to the two sides of bilayer membrane surface
Figure 1 contains a graph of c ? c1
for the four systems PC–Val (Fig. 1a), PC–Ile (Fig. 1b),
PC–Tyr (Fig. 1c), and PC–Phe (Fig. 1d). According to
Eq. 2, when the membrane components do not interact
these functions should yield straight lines. This is clearly
not the case, which suggests that a complex or other
structure exists in PC–Val, PC–Ile, PC–Tyr, and PC–Phe
bilayers. Because the use of Eq. 3 presupposes the exis-
tence of 1:1 complexes, our initial assumption was that the
complexes formed were 1:1. The interfacial tension of the
lipid membrane was studied over a wide range of lipid
Equation 2 predicts that in the absence of interactions, the
plot of Fig. 1a should yield a straight line. The nonlinear
phosphatidylcholine and valine. Such interactions in phos-
phatidylcholine–amino acid systems in monolayer can be
explained in terms of complexes . The 1:1 complex is
formed in the initial stage of complexation, followed by
other compositions in subsequent stages. In our case, an
equation derived to describe the equilibrium of 1:1 complex
formation was sufficient for the entire concentration range.
Figure 2a depicts the interfacial tension of a PC–Val
membrane as a function of valine mole fraction. The
dependences of interfacial tension of lipid membranes
formed from the PC–Val system was executed in the
function of the composition to 60% of the valine contents,
because only to such contents of component 2 (valine) with
lecithin were the forming bilayer membrane.
The interfacial tension value of pure lecithin membrane
(component 1), c1was measured directly and presented
earlier ,whichisequal1.62 9 10-3N m-1.There isno
accurate literature data on interfacial tension values for the
pure amino acid (valine, isoleucine, tyrosine, and phenyl-
alanine), because these components are not creating the
bilayer membrane. However, in order to characterize the
course of the experimental curves, the c2value for the pure
components are necessary, which will be used for calcula-
tion. In this case, the interfacial tension hypothetical values
for membranes built from amino acids were determined
adjusting the experimental curve with the polynomial of the
other mark extrapolating the x2= 1 value. An example of
this extrapolation for valine membrane is presented in
pure valine, isoleucine, tyrosine, and phenylalanine are
292Cell Biochem Biophys (2011) 61:289–296
equal to 7.0 9 10-4, -2.7 9 10-3, -3.5 9 10-3, and
5.3 9 10-3N m-1, respectively. Negative values of inter-
facial tension for membrane built from pure isoleucine and
the bilayer membrane from pure amino acid. Thermody-
namic potential forthis bilayer would have a negative value,
i.e., the bilayer is not forming.
The valine and phenylalanine membrane interfacial
tension value is positive. However, it is not possible to
create a bilayer lipid membrane from the pure component
because the forming solution above 60% of valine or 25%
of phenylalanine was granulated in the solution.
Based on the literature, an assumption was made that
a 1:1 complex (termed compound 3) formed the most
prevalent structure and was characterized by a maxi-
mal stability constant K . Given this assumption,
the dependence of interfacial tension on the composition of
the membrane-forming solution is described by Eq. 3. The
interfacial tensions of membranes formed from the pure
components were experimentally or theoretically deter-
mined. The constants B1;B2 and c3were determined
assuming that the value of the stability constant for the PC–
Val complex was sufficient with respect to the simplified
Eq. 3 to Eqs. 4 and 5.
Fig. 1 Graph of Eq. 2 for
tyrosine (c), and
phenylalanine (d), where x2is
the mole fraction of component
2 (valine, isoleucine, tyrosine,
γ, N m-1
γ , N m-1
γ , N m-1
0 0,20,4 0,60,81
00,2 0,40,6 0,81
0 0,20,4 0,6 0,81
γ, N m-1
Fig. 2 The interfacial tension c
(c), and phosphatidylcholine–
phenylalanine (d), as a function
of mole fraction x2of
component 2 (the experimental
values are marked by points and
the theoretical values are
indicated by the curve)
Cell Biochem Biophys (2011) 61:289–296293
Graphs of functions (4—denoted by 1) and (5—denoted
(1.505) were determined from the slopes of the lines. The
intersections of the straight lines with the ordinate provide
?B1c3and ?B2c3, which can be used to determine c3, the
interfacial tension of the PC–Val complex. The mean value
obtained in this way was 2.04 9 10-3N m-1.
Determining the interfacial tension as a function
of compositionenabled the
concentrations for membranes formed of pure components.
At least one of these calculations is necessary to determine
the value of A?1
phosphatidylcholine and valine are 85 A˚2mol-1 and
155 A˚2mol-1(accessible surface area calculated for
the residue X in the tripeptide G–X–G ), respectively.
The surface concentrations of phosphatidylcholine and
valine in membranes of pure components, calculated from
surface area presented above, are 1.96 9 10-6
1.07 9 10-6mol m-2. Knowing A?1
and B2, the surface concentration of a membrane composed
of PC–Val complex can be determined. The resulting sur-
face concentration value A?1
6.89 9 10-7mol m-2. From this it was possible to deter-
mine that the area occupied by one PC–Val complex is
approximately 241 A˚2mol-1. The surface area value
(85 A˚2mol-1), but is almost equal the sum of the areas of
phosphatidylcholine and valine (240 A˚2mol-1).
The stability constant of the phosphatidylcholine–valine
complex was determined from Eq. 6 by setting x1¼
x2¼ 0:5. The stability constant was 1.32 9 108m2mol-1.
Knowing the stability constant value, the complex forma-
tion energy (Gibbs free energy) of a membrane composed
of PC–Val complex can be determined. This value is equal
-49.02 ± 1.47 kJ mol-1.
3. The surface areas occupied by
2as well as B1
for the PC–Val complex was
The dependence of lipid membrane interfacial tension on
composition for PC–Ile, PC–Tyr, and PC–Phe systems
were studied over a possible concentration range. The
results are depicted in Fig. 2b–d. The dependences of
interfacial tension of lipid membranes formed from the
PC–Ile, PC–Tyr, and PC–Phe systems were executed in the
function of the composition to 41% of the isoleucine
contents (to 26% of the tyrosine and to 25% of the phen-
ylalanine), because only to such contents of component 2
(isoleucine, tyrosine, phenylalanine) with lecithin were the
forming bilayer membrane.
The values of c3for the PC–Ile, PC–Tyr (1.91 9 10-3,
1.75 9 10-3N m-1), and PC–Phe (3.69 9 10-3N m-1)
complexes were calculated using Eqs. 4 and 5. Equations 4
and 5 could also be used to calculate the surface concen-
trations per unit area of membranes formed entirely from
PC–Ile, PC–Tyr, and PC–Phe complexes (the surface area
occupied by isoleucine, tyrosine, and phenylalanine are
175, 230, and 110 A˚2mol-1, respectively  and the
surface concentration calculated for pure isoleucine, tyro-
sine, and phenylalanine membranes are 9.49 9 10-7,
7.22 9 10-7, and 1.51 9 10-6mol m-2, respectively).
From these values it is possible to determine the areas
y = -0,0027x + 0,0034
R2 = 0,9887
γ ,N m-1
Fig. 3 A plot illustrating the hypothetical interfacial tension values
for valine membrane calculation
γ, N m-1
(γ1-γ)/(x1-x2), N m-1
0,0E+00 1,0E-032,0E-033,0E-034,0E-03 5,0E-036,0E-03
γ, N m-1
(γ2-γ)/(x2-x1), N m-1
Fig. 4 A plot illustrating Eq. 4 (1) and Eq. 5 (2) for calculating the
parameters B1, B2, c3(for phosphatidylcholine–valine system)
294Cell Biochem Biophys (2011) 61:289–296
occupied by PC–Ile, PC–Tyr, and PC–Phe complexes,
which are 310, 398, and 219 A˚2mol-1. The surface area
values obtained in this way are higher than the area of a PC
molecule, but are almost equal the sum of the areas of
phosphatidylcholine and amino acid.
The stability constants of the PC–Ile, PC–Tyr, and PC–
Phe complexes were determined using Eq. 6. The stability
constant of PC–Ile complex is 1.97 9 107m2mol-1, and
the constants PC–Tyr and PC–Phe are 5.36 9 107and
1.29 9 105m2mol-1. It should be emphasized that the
stability constant of phosphatidylcholine–tyrosine and
phosphatidylcholine–phenylalanine are higher for com-
plexes in bilayers than in the same systems in monolayer
(K = 6.04 9 105m2mol-1for PC–Tyr and K = 1.39 9
105m2mol-1for PC–Phe complexes) . A monolayer
is a two-dimensional system forming a plane at the air/
water interface, while a bilayer possesses a third dimen-
sion, and is additionally stabilized by hydrophobic inter-
actions between the hydrocarbon chains.
Knowing the stability constant values, the complex for-
of PC–Ile, PC–Tyr, and PC–Phe complexes can be deter-
mined. These values are equal -44.03 ± 1.32, -46.97 ±
1.39, and -30.85 ± 0.93 kJ mol-1, respectively.
The experimental values inFig. 2b, care markedbypoints,
and the theoretical ones obtained from Eq. 7 are marked by
lines. It can be seen from these figures that the agreement
between experimental and theoretical points are good, which
verifies the assumption of a formation of 1:1 PC–Ile, PC–Tyr,
and PC–Phe complexes in the lipid membranes.
Table 1 lists several physicochemical parameters for
membranes containing PC–Ile, PC–Tyr and PC–Phe
The analysis of the results presented in Table 1 leads to
the following conclusions:
1. The stability constant of the PC–Val complex is
1.32 9 108m2mol-1, whereas the stability constant of
the PC–Ile, PC–Tyr, and PC–Phe complexes are
1.97 9 107, 5.36 9 107, and 1.29 9 105m2mol-1,
respectively.These values arerelatively high,
providing additional support for the prevalence of
1:1 complexes in mixed bilayers. These values also
confirm that the assumption used to simplify Eq. 1 was
correct. This paper contains the first report of stability
constants for PC–Val, PC–Ile, PC–Tyr, and PC–Phe
The complex formation energy (Gibbs free energy)
values for the PC–Val, PC–Ile, PC–Tyr, and PC–Phe
complexesare-49.02 ± 1.47,-44.03 ± 1.32,-46.97
± 1.39, and -30.85 ± 0.93 kJ mol-1, respectively.
Good agreement between the experimental and theoret-
ical points verifies the assumption of only 1:1 complex in
the lipid membrane. The lack of variation between
theoretical and experimental points indicates that our
theoretical model (presented in the ‘‘Theory’’ section) is
sufficient to describe the interaction in phosphatidylcho-
line–amino acids systems. The agreement between the
experimental results and model predictions for the
PC–Val, PC–Ile, PC–Tyr, and PC–Phe membranes
justifies the statement that other complexes do not
represent a significant component of these systems.
The mathematically derived and experimentally con-
the interpretation of phenomena occurring in lipid
bilayers. These results can help lead to a better
understanding of the physical properties of biological
membranes. The simple and very interesting methods
proposed in this paper and in earlier studies [11–14, 23]
may be used with success to determine the equilibrium
constant values of 1:1 lipid–lipid, lipid–cholesterol,
lipid–fatty acid, lipid–amine, and lipid–amino acid
Creative Commons Attribution Noncommercial License which
permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are
This article is distributed under the terms of the
Table 1 Selected physicochemical parameters for four complexes: phosphatidylcholine–valine (PC–Val), phosphatidylcholine–isoleucine
(PC–Ile), phosphatidylcholine–tyrosine (PC–Tyr), and phosphatidylcholine–phenylalanine (PC–Phe)
Examined systemSurface area occupied
by one molecule
of complex (A˚´2molecule-1)
of examined complex
energy (Gibbs free energy)
PC–Val 241 ± 2.411.32 9 108
1.97 9 107
5.36 9 107
1.29 9 105
-49.02 ± 1.47
PC–Ile310 ± 3.10
-44.03 ± 1.32
PC–Tyr398 ± 3.99
-46.97 ± 1.39
PC–Phe219 ± 2.19
-30.85 ± 0.93
Cell Biochem Biophys (2011) 61:289–296295
References Download full-text
1. Przestalski, S. (1983). Błony biologiczne. Warsaw: Wiedza
2. Popova, A. V., Heyer, A. G., & Hincha, D. K. (2002). Differential
destabilization of membranes by tryptophan and phenylalanine
during freezing: the roles of lipid composition and membrane
fusion. Biochimica et Biophysica Acta, 1561, 109–118.
3. Zarandi, M. (2007). Amino acids. Amino Acids, Peptides and
Proteins, 36, 19–81.
4. von Heijne, G. (2007). Formation of transmembrane helices in
vivo-is hydrophobicity all that matters? Journal of General
Physiology, 129, 353–356.
5. White, S. H. (2007). Membrane protein insertion: the biology–
physics nexus. Journal of General Physiology, 129, 363–369.
6. Wolfenden, R. (2007). Experimental measures of amino acid
hydrophobicity and the topology of transmembrane and globular
proteins. Journal of General Physiology, 129, 357–362.
7. MacCallum, J. L., Bennett, W. F. D., & Tieleman, D. P. (2008).
Distribution of amino acids in a lipid bilayer from computer
simulations. Biophysical Journal, 94, 3393–3404.
8. MacCallum, J. L., Bennett, W. F. D., & Tieleman, D. P. (2007).
Partitioning of amino acid side chains into lipid bilayers: results
from computer simulations and comparison to experiment.
Journal of General Physiology, 129, 371–377.
9. Jacobs, R. E., & White, S. H. (1989). The nature of hydrophobic
binding of small peptides at the bilayer interface: implications
for the insertion of transbilayer helices. Biochemistry, 28,
10. Brown, J. W., & Huestis, W. H. (1993). Structure and orientation
of a bilayer-bound model tripeptide: A proton NMR study.
Journal of Physical Chemistry, 97, 2967–2973.
11. Petelska, A. D., Naumowicz, M., & Figaszewski, Z. A. (2006).
The interfacial tension of the lipid membrane formed from lipid-
cholesterol and lipid-lipid systems. Cell Biochemistry and Bio-
physics, 44, 205–212.
12. Petelska, A. D., Naumowicz, M., & Figaszewski, Z. A. (2007).
Interfacial tension of the lipid membrane formed from lipid-fatty
acid and lipid-amine systems. Bioelectrochemistry, 70, 28–32.
13. Petelska, A. D., & Figaszewski, Z. A. (1998). Interfacial tension
of the two-component bilayer lipid membrane modelling of cell
membrane. Biolectrochemistry and Bioenergetics, 46, 199–204.
14. Petelska, A. D., Naumowicz, M., & Figaszewski, Z. A. (2006).
Physicochemical insights into equilibria in bilayer lipid mem-
branes. In H. T. Tien & A. Ottova (Eds.), Advances in planar
lipid bilayers and liposomes (Vol. 3, pp. 125–187). Amsterdam:
15. Inczedy, J. (1976). Analytical applications of complex equilibria.
Budapest: Akademiai Kiado.
16. Adamson, A. W. (1960). Physical chemistry of surfaces. New
York: Interscience Publishers Inc.
17. Petelska, A. D., & Figaszewski, Z. A. (2000). Effect of pH on the
interfacial tension of lipid bilayer membrane. Biophysical Jour-
nal, 78, 812–817.
18. Mueller, P., Rudin, D. O., Tien, H. T., & Wescott, W. C. (1963).
Method for the formation of single bimolecular lipid membranes
in aqueous solution. Journal of Physical Chemistry, 67, 534–535.
19. Benz, R., Frohlich, O., Lauger, O., & Montal, M. (1975). Elec-
trical capacity of black films and of lipid bilayers made from
monolayers. Biochimica et Biophysica Acta, 374, 323–334.
20. Karolins, C., Coster, H. G. L., Chilcott, T. C., & Barrow, K. D.
(1998). Differential effects of cholesterol and oxidized-choles-
terol in egg lecithin bilayers. Biochimica et Biophysica Acta,
21. Petelska, A. D., Naumowicz, M., & Figaszewski, Z. A. (2011).
The equilibrium of phosphatidylcholine-amino acid system in
monolayer at the air/water interface. Cell Biochemistry and
22. Chothia, C. (1976). The nature of the accessible and buried sur-
faces in proteins. Journal of Molecular Biology, 105, 1–12.
23. Petelska, A. D., Naumowicz, M., & Figaszewski, Z. A. (2009).
Complex formation equilibria in two-component bilayer lipid
membrane: interfacial tension method. Journal of Membrane
Biology, 228, 71–77.
296Cell Biochem Biophys (2011) 61:289–296