THE ROLE OF COUNTERIONS IN THE INTERACTION OF BIFUNCTIONAL SURFACE ACTIVE COMPOUNDS WITH MODEL MEMBRANES
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1 Vol. 44, No. 6, May 1998 BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL Pages THE ROLE OF COUNTERIONS IN THE INTERACTION OF BIFUNCTIONAL SURFACE ACTIVE COMPOUNDS WITH MODEL MEMBRANES Sarapuk J., Kleszczyfiska H. and R6Zycka-Roszak B. Department of Physics and Biophysics, Agricultural University, Norwich 25, Wroctaw, Poland Received December 30, 1997 Received after revision, January 19, 1998 Smmnm-y Interaction of two series of bifunctional surfactants (bromides and chlorides) with red blood cells and planar lipid membranes was studied. The aim of the work was to determine the role of counterions in the mechanism of interaction of bifunctional cationic surfactants with model membranes. In each case bromides influenced model membranes to a greater degree than the corresponding chlorides. The possible explanation of the obtained results is presented. It seems that the greater ability of bromides to destabilize model membranes in comparison with chlorides can be attributed to the greater mobility and the smaller radius of the hydrated bromide ion. This may underlie the greater ease that this anion can modify the surface potential of the lipid bilayer, thus enhancing the interaction of the cationic surfactant with such a modified bilayer. Introduction The effectiveness of the interaction of amphiphilic substances with model membranes depends on many different factors. These are polarity, which depends on steric effects of the polar head of the compound, its net charge or charge distribution, and lipophilicity which depends, in turn, on the number and length of alkyl chains of an amphiphilic compound (1,2). In the latter case it is also important if there are any intermediate groups incorporated between the polar head of a compound and its lipophilic alkyl chain(s) or, as happens in the case of so-called gemini compounds, interspatial groups incorporated between the polar heads of such substances (3,4,5). The above formulated conclusions apply also to the biological activity of these substances (6,7,8,9). However, it was found in both biological and model experiments on the interaction of amphiphilic /98/061105~ /0 Copyright by Academic Press Australia. All rights of reproduction in any form reserved.
2 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL compounds with membranes that the type of counterion can be an important factor influencing the interaction (10,11,12), The paper contains some results obtained on the interaction of a series of chlorides and bromides of bifunetional surfactants with model membranes (planar lipid membranes and erythrocytes). They were synthesized to be used preferentially as biologically active compounds or antioxidant agents, as they have a free radical scavenging group incorporated in their polar head. In their second protective role they must be used in a proper concentration range. Too high a concentration can lead to changes and/or disruption of the membrane of the protected object (12). The aim of the work was twofold: to fmd whether there is any difference in the interaction of chlorides and bromides of the surfactant studied with model membranes, and to formulate a hypothesis explaining the differece in the interaction if found. Materials and Methods Fresh heparinized pig erythrocytes were used in hemolytic experiments. The blood was centrifuged for 3 min at 1000 g~ the plasma was removed and the cells were washed four times with an isotonic phosphate solution of ph 7.4 (131 mm NaC1, 1.79 mm KC1, 0.86 mm MgCI2, mm Na2HPO4-2H20, 1.80 mm NaH2PO4-H20). The erythrocytes were then treated for half an hour at 37 ~ with the same solution containing different concentrations of the compounds studied. Four different hematocrits were used. After modification samples were taken, centrifuged and the supernatant was assayed for hemoglobin content using a Spekol 11 (Carl Zeiss, Jena) spectrophotometer at 540 nrm A measure of the extent of hemolysis was the hemoglobin concentration in the supernatant of totally hemolyzed cells. Planar lipid membranes (BLM) were formed from a solution of 1.5% (w/v) azolectin (Sigma Chem. Co.) in n-butanol:n-decane (1:1) on a 1.7 mm hole in the partition of a twocompartmental chamber filled with 0.9 % NaC1 solution. The compounds studied were pipetted into measurement chamber until their concentrations reached values that caused BLM breakdown in no more than 5 min. These concentrations are farther on referred as critical concentrations ((2(2). The bifunctional ammonium chlorides of the general formulas shown in Fig. 1 were synthesized in the Institute of Organic and Polymer Technology, Technical University, Wroctaw, Poland. Their purity and structure were checked by NMR spectra and elemental analysis. Results Typical results of the hemolytic experiments are shown in Fig. 2 for C9H19 and C16H33 alkyl chain bromides. Hemolytic curves made it possible to estimate of the concentrations of the compounds causing 100% hemolysis (C~0o). Such approach was 1106
3 BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL HO-~CH2 n = 9, 12, 14, ~+ (CH3)2 CnH2n+1 Br- HOOCH2 n = 9, 12, 14, 16 --N + (CH3)2 I CH2OCnH2n+I Cl- HOOCH2 --!+ --CH3 CI- Fig. 1 HO H I CH2--N +- CH3 t C12H25 General formulas of the bifunctional surfactants studied. Br- chosen because the C10 0 is qualitatively similar to the CC parameter determined in BLM experiments. Namely, both parameters describe total membrane disruption. Estimated values of C10 0 are shown in Table 1. Azolectin BLMs used in the experiments were highly stable in the absence of the surfactants studied. This stability gradually decreased as surfactant concentration in the bath solution increased. The obtained values of critical concentrations (CC) of compounds, i. e., concentrations causing destruction of BLMs in less than 5 rain. are shown in Table 2. Discussion Both BLM and erythrocyte studies showed that the bifunctional surfactants studied here act as destabilizers of model membranes when used at high enough concentrations. In both cases the destruction of membranes depended on the length of the hydrophilie part of the compounds studied. It also depended on the kind of counterion of a cationic 1107
4 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL 100 A.~-~ 2J J;,~,~ B H=2% rj O A H=4% H=6% H=8% O E -1" ,00 Concentration [mm] Fig. 2 Dependence of the degree of red blood cell hemolysis on concentration of -C9H19 and -Cl6Hs3 alkyl chain bromides. Table 1 Concentrations of the compounds studied that cause 100% hemolysis of red blood cells (Cl00). Alkyl chain qoo [MI Hematocrit Bromides -C12H2s "C14H29 -C16H33 2% "10 4 4% 9.0 " " " "10 4 6% "s 8.5 " " % 14.4 "10 "s Chlorides -c9hi, -C12H2s -C14H29 -C16H _ 1.6"10 "~ 5.5 " o o.-r 2.0" " " "~ i0 "~ 2.7" 10 s s
5 BIOCHEMISTRY end MOLECULAR BIOLOGY INTERNATIONAL Table 2 Critical concentrations (CC) of the compounds studied. Alkyl chain/group Chlorides cc [M] Bromides -C9H19 -C12H25 "C14H29 -C16H33 -H " " " " surfactant. Bromide compounds were fbund to be more efficient in destabilizing the model membranes than the chloride ones. It seems, on the basis of the results obtained for both model membranes, that the greater efficiency in membrane destabilization by bromide surfactants in comparison with that observed for chloride surfactants is more evident for compounds possessing shorter hydrophobic chains. Electrostatic interaction between the polar heads of a lipid and surthctant may be an important factor in such cases. In contrast, amphiphilic surfactant molecules with long hydrophobic parts can incorporate into membranes so deeply that the hydrophobic interaction between the alkyl chains of lipid and surfactant nmlecules is a dominant factor in the overall interaction as was shown earlier (2). In line with such an approach one can assume that bromide ions can modify the electrostatic properties of the model menabrane surface to a greater extent than chloride ions can,. enabling the surfactant to interact more strongly with those membranes. Similar results pointing to stronger modifying possibilities of bromides were fbund in monolayer studies on cationic and anionic surfactants and their mixtures (13,14,15). It was shown in these experiments that at a constant concentration of inorganic ions there is higher cationic surfactant adsorption to cationic-anionic monolayers tbr NaBr than for NaC1. The difference in the effects of ions of the same valency is explained by their different binding to charged surfaces resulting from their different polarizability or hydration and mobility (16). The smaller effective radius of the bromide ion permits it to bind more strongly to positively charged groups of membrane surfaces and by weakening the electrostatic interaction to 1109
6 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL facilitate the incorporation of a cationic surfactant into the membrane. Even an elongation of the hydrophobie part of a chloride surfactant by incorporating an the intermediate oxymethylene group, corresponding to two methylene groups (3), between the hydrocarbon chain and polar head of the surfactant and the eiflaancened hydrophobic interaction with model membranes cannot make the chloride surfactant more effective than the bromide one in destabilizing the membranes. Acknowledgement. This work was sponsored by the Polish Research Committee (KBN), grant no. P04G References I. Sarapuk J., Kleszczyfiska H., Przestalski S., Witek S. (1986) studia biophysica, 113, Kleszczyfiska H., Sarapuk J., Przestalski S., Kilian M. (1990) studia biophysica, 135, Sarapuk J., Gabrielska J., Przestalski S. (1992) Polish J. Era,iron. Studies 1, Gabrielska J., Sarapuk J., Przestalski S. (1994) Tenside Surf. Det. 31, Przestalski S., H/adyszowski J., Kuezera J., R6L2ccka-Roszak B., Trela Z., Chojnacki H., Witek S., Fisicaro E. (1996) Biophys. J. 70, i. 6. Ashman R.B., Blanden R.V., Ninham B.W., Evans D.F. (1986) Immunology Today, '7, Devinsky F., Kopecka-Leitmanova A~, Sersen F., Balgavy P. (1990) J. Phman. Pharmacol. 42, Trela Z., Janas T., Witek S., Przestalski S. (1990) Physiol. Plant. 78, Balgavy P., Devinsky F. (1994) XIIth School on Biophysics of Membrane Transport, Zakopane Poland, School Proceedings, ( Przestalski, S., Kuczera, J., mad Kleszczyfiska, H., Eds.) part I, pp Witek S., O~wi~cimska M., Lachowicz T.M., Batakuszew A~, Przestalski S., Kuezera J., Sarapuk J., Kleszczyfiska H., Gabrielska J., H~adyszowski J., Trela Z., Kral T., Podolak M. (1994) Folia Microbiol. 6, Gabrielska J., Sarapuk J., Przestalski S. (1995) Z. Naturforsch. 50c, Sarapuk J., Gabrielska J., Przestalski S. (1997) Current Topics Biophys. 21, G6ralczyk D. (1991) Colloids Surf. 59, G6ralczyk D. (1993) Tenside SurE. Det. 30, G6ralczyk D. (1994) L Coll. Interface Sci. 167, Dolowy K. (1997) XIIIth School on Biophysics of Membrane Transport, L~dek Zdr6j, Poland, School Proceedings ( Kuczera, J., Kubica, K., R6~ycka-Roszak, B., and Przestalski, S. Eds.), part I,
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