BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL
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1 Vol. 45, No. 4, July 1998 Pages INTERACTION OF SODIUM BIS(2-ETHYLHEXYL) SULFOSUCCINATE (AOT) WITH CATALASE AND HORSERADISH PEROXIDASE IN AN AQUEOUS SOLUTION AND IN THE REVERSE MICELLES OF AOT/N-HEPTANE Lidia G~bicka, Jerzy L. G~bicki Institute of Applied Radiation Chemistry, Technical University of L6dL WrOblewskiego 15, L6d~, Poland Received April 16, 1998 Summary Some properties of catalase and horseradish peroxidase entrapped into reverse micelles of sodium bis(2-ethylhexyl) sulfosuccinate (AOT)/n-heptane with those in an aqueous solution of AOT are compared. Secondary structure of catalase significantly changes and activity is completely lost in the presence of aqueous micellar solution of AOT. In AOT/n-heptane reverse micelles secondary structure of catalase does not change. AOT has no effect on horseradish peroxidase in aqueous solution. On the other hand slight changes in secondary structure &horseradish peroxidase in AOT/n-heptane reverse micelles appear. It is concluded that electrostatic interactions between catalase or horseradish peroxidase with AOT molecule at neutral ph are not the main factor determining reactivity of investigated enzymes in reverse micelles. Key words: horseradish peroxidase catalase electrostatic reverse micelles interactions Introduction Reverse micelle which are formed by certain amphiphilic molecules in apolar solvents can entrap water and hydrophilic molecules, including proteins, within their hydrophilic core. It is generally accepted that a layer of water separates and protects the protein surface from the inner surface of the surfactant layer. On the other hand, a high charge density of the surfactant layer is the reason of anomalous properties &water which may influence the structure of entrapped proteins (1-3). It was also suggested, that even in the case ofhydrophilic proteins, which are located exclusively in the water pool, the electrostatic interaction &the charged Abbreviations used: ABTS, 2,2'-azino-bisl3-ethyl-benzoth!azoline-(6)sulphonic acid; AOT, sadiron bis(2- ethylhexyl) sulfosuccinate /98/ / Copyright by Academic Press Australia. All rights of reproduction in any form reserved.
2 residues of the protein with the charges of surfactant molecules forming reverse micelles is of considerable importance to the protein structure. Takeda et al. (4) showed that the secondary structural change of bovine serum albumin incorporated into reverse micelle of anionic surfactant, sodium bis(2-ethylhexyl) sulfosuccinate, AOT, phenomenologically resembles that observed in the aqueous solution of this surfactant or in an other anionic surfactant, sodium dodecyl sulphate (SDS). They also showed several examples of proteins in which changes of helicities were the same in AOT reverse micelles as in aqueous solution of SDS. It was reported that some enzymes incorporated into reverse micelles of AOT show,,superactivity" (5). Heme enzymes, catalase and horseradish peroxidase are among them (6-9). On the other hand anionic surfactants in aqueous solutions are known to bind to the proteins what may lead to their denaturation. Very recently we have shown that while horseradish peroxidase is slowly inactivated in the presence of SDS aqueous micelles, catalase undergoes rapid inactivation in the presence of this surfactant (1). In this work we compare properties of both enzymes entrapped into the reverse micelles of AOT/n-heptane with those in an aqueous solution of AOT. Our data show that in the case of catalase and horseradish peroxidase, at neutral ph, electrostatic interaction with AOT forming reverse micelle have, if any, insignificant influence on enzyme structure in reverse micelles. Experimental Bovine-liver catalase (twice crystallized), RZ =.8, and horseradish peroxidase type VI A, RZ = 3. were obtained from Sigma. Extinction coefficients of 3.24 x 15 M 1 cm "x at 45 nm (11), and 1.2 x 15 M 1 cm 1 at 43 nm (12) were used for spectrophotometric determinations of catalase and horseradish peroxidase concentrations, respectively. The activity of catalase was determined by the method of Beers and Sizer (13). The activity of horseradish pero was assayed using 2,2'-azino-bis[ethyl-benzothiazoline-(6)-sulphonic acid] (ABTS) (14). Water from MilliQ Plus (Millipore) was used throughout. Sodium bis(2-ethylhexyl)sulfosuccinate (AOT) from Sigma was dried under vacuum over P25. AOT reverse micelles were formed by injection of appropriate amounts of aqueous stock solutions in 1 mm phosphate buffer, ph=7. into.1 M AOT in n-heptane (Sigma, puriss) to obtain desired Wo, i.e the ratio of [H2] to [AOT], where water indicates the buffer alone or buffer containing protein. The mixture was shaken until a completely transparent solution was obtained. Aqueous solution of AOT in 1 mm phosphate buffer, ph=7..was also used as a solvent for investigated proteins. Critical micelle concentration (CMC) in 1 mm phosphate buffer as determined by speetrophotometric method, using acridine dye as a probe (14) was 2.3 ram. 86
3 BIOCHEMISTRYand MOLECULAR BIOLOGY INTERNATIONAL CD experiments were performed on CD 6 Jobin Yvon dichrograph, using.1 cm cells for the far ultraviolet range of 25-2 nm. Absorption spectra and kinetic measurements of enzyme activity were done on Hewlett-Packard 8452A diode-array spectrophotometer. Results and discussion We have observed that catalase totally looses its activity after 24 h incubation with aqueous solution of AOT at concentrations above 2.5 mm i.e. above CMC (Table 1). Intensity of the absorption maximum of catalase (45 nm) is lowered already in the presence of AOT at concentration below CMC and additionally is blue shifted to 398 nm in the presence of AOT micelles (Table 1). Fig. 1 shows far-uv CD spectrum of catalase taken in the presence of aqueous solution of AOT. As one can see, any changes are observed in the presence of.8 mm of AOT. Changes in CD spectrum of catalase appear after 24 h incubation with 8 mm AOT. The spectrum is nearly identical with CD spectrum of catalase in an aqueous solution of SDS micelles (1). A negative band at 222 nm is reduced indicating that the content of~-helical conformation is lower. It means that AOT in an aqueous solution is a denaturing agent for catalase. According to Takeda et al. (4) this may be accounted for the binding of this surfactant to the catalase molecule. They showed that the helicity of bovine serum albumin decreased in the same concentration range of AOT in water as the binding of AOT to the protein proceeded (4). Far-UV CD spectra of catalase incorporated into reverse micelles of AOT in n-heptane do not significantly change in respect to far-uv CD spectrum of catalase in an aqueous solution (data not shown). Similar observations published earlier Haber et al. (7) for catalase incorporated into reverse micelles of AOT in isooctane. The rate of H2Oz decomposition by catalase, however, increases significantly upon introduction of reactants into AOT/n-heptane reverse miceues under the same overall concentrations as in aqueous solution. It is by 2% higher at wo=2 and threefold higher at Wo=5 than that in homogeneous aqueous solution. The results are in accordance with those for catalase in AOT/isooctane reverse micelles (7). It means that the kind of hydrocarbon has no effect on the enzymatic reaction. The efficiency of substrate supply in reverse miceuar system is limited by the exchange process between substrate-filled and enzyme-filled micelles. For AOT as a surfactant, exchange occurs with a second-order rate constant of M "1 s "1 (16). As the values of the overall rate constant 87
4 Table 1. The influence of AOT concentration in water on the relative activity X... and absorbance at ~,,, of catalase measured after 24 h incubation at 8 ~ [AOTI (mm) Relative activity (%) ~m.x Absorbance at ~max OO -3OO -4O3O -5OO -6OO -7 I I, I, I, I, Wavelength / nm Fig. 1. Far-UV CD spectra of.7 ~tm catalase in buffer solution, ph ~ 7. (solid line) and in the presence of.8 mm (dashed line) or 8 mm (dotted line) AOT in buffered aqueous solution (ph = 7.). 88
5 BIOCHEMISTRYand MOLECULAR BIOLOGY INTERNATIONAL 33-4OO -6 ' ~ I, I, I ~ I, Wavelength / nm Fig. 2. Far-UV CD spectra of 4 #M horseradish peroxidase in buffer solution, ph = 7. (solid line) and in AOT/n-heptane reverse micelles ofwo = 1 (dashed line), Wo = 2 (dotted line) and Wo = 3 (-..- line). for beef liver catalase fall between.6 and 2 x 17 M 4 s "1 (17), i.e. are comparable with the exchange rate constant, it was suggested that the exchange of reverse micelles becomes the rate-limiting step in the decomposition of H2Oz catalyzed by catalase in reverse micelles (7). Very high local concentrations of catalase and H22 within small water droplet confined in reverse micelles causes that chemical step occurs immediately after reagents meet. It was found that the second investigated enzyme, horseradish peroxidase, oxidizes ABTS in AOT/n-heptane reverse micelles with the rate of about one order of magnitude higher than that observed in homogeneous aqueous solution under the same overall reagents concentrations (18). Fig. 2 shows far-uv CD spectra of horseradish p eroxidase in AOT/n-heptane reverse micelles. Horseradish peroxidase molecule is slightly unfolded in micelles at Wo = 1, but retains native-like structure barely at Wo = 3. If changes of horseradish peroxidase conformation originate mainly from electrostatic interactions between AOT molecules and horseradish peroxidase solubilized in the interior of reverse micelles, some alterations in secondary structure of horseradish peroxidase would be observed in aqueous solution of the same surfactant. It is not the case, the absorption and far-uv CD spectra of 89
6 native horseradish peroxidase in buffer solution (ph = 7.) and in aqueous buffered AOT solution (ph = 7.) below and above micellar concentration are very similar (data not shown). As one can expect, full activity &horseradish peroxidase in AOT aqueous solution is retained. Turning back to horseradish peroxidase in reverse micelles, the rate constant of the slowest reaction in horseradish peroxidase cycle of ABTS oxidation was found to vary from 1.3 x 16 for wo < 17 to.7 X 16 M "1 s "1 for wo > 17 (5.1 x 14 M -1 s "1 in homogeneous aqueous solution) (18). It seems that, contrary to catalase, exchange of solubilizates is not the only factor determining the rate of the overall process. Quite likely the effect of partial enzyme inactivation, which may occur at lower Wo is superimposed on the concentration effect in the water pool (the higher Wo the lower water-pool concentration). The presence of bound water, the fraction of which is high at low Wo, could also influence the chemical step in horseradish peroxidase cycle. We belive that ifaot in aqueous solution at ph 7. does not modify HRP, it will be also inactive towards horseradish peroxidase in reverse micelles (assuming that ph does not significantly change in the water pool). Taking into account the above results we conclude that for catalase and horseradish peroxidase, contrary to several other proteins, the electrostatic interactions with AOT molecules are not the main factor determining reactivity of investigated enzymes in reverse micelles at neutral ph. Whereas horseradish peroxidase appears relatively resistant against anionic surfactants (1), catalase undergoes denaturation by AOT in homogeneous aqueous solution. It seems that the presence of bound water in the water pools of reverse micelles effectively protects catalase molecule from the denaturing effect of the surfactant molecules. Acknowledgements This work was supported in part by the Polish Committee of Scientific Research (KBN grant 3T9A 113 9). The CD measurements have been possible thanks to the Foundation of Polish Science which supported in whole the purchase of the apparatus. The authors thanks Mrs. M. Boczkowska from the Centre of Molecular and Macromolecular Studies, Polish Academy of Sciences, L6d2, for performing CD measurements. References 1. Barbaric, S. and Luisi, P. L. (1981) J. Am. Chem. Soc. 13, Luisi, P. L. (1985) Angew. Chem. Int. Ed. 24, Vos, K., Laane, C., Weijers, S. R., Van Hock, A., Veeger, C. and Visser, A. J. W. G. (1987) Eur. J. Biochem. 169,
7 4. Takeda, K., Harada, K., Yamaguchi, K. and Moriyama Y. (1994) J. Colloid Interface Sci. 164, Martinek, K., Levashov, A. V., Klyachko, N., Khmelnitski, Yu. L. and Berezin, I. V. (1986) Eur. J. Biochem 155, Artiomchik, W. D., ErjomJn, A. N. and Metelitza, D. I. (199) Biokchimija 55, Haber, J., Ma~lakiewicz, P., Rodakiewicz-Nowak, J. and Walde, P. (1993) Eur. J. Biochem. 217, Martinek, K., Levashov, A. V., Klyachko, N., Khmelnitski, Yu. L. and Berezin, I. V. (1982) Science 218, Eryomin, A. N. and Metelitza, D. I. Biokhimija 5, G~bicka, L. submitted for publication. 11. Samejima, N. and Yang, J. (1963) J. Biol. Chem. 238, Ohlsson, P. J. and Paul, K G. (1976) Acta Chem. Scand. B3, Beers, R. F. and Sizer, J. W. (1952) J. Biol. Chem. 195, Childs, G. V. and Bardsley, W. G. (1975) Riochem J. 145, Corrin, M. L. and Harkins, W. D. (1947) J. Am. Chem. Soc. 69, Fletcher, P. D. I., Howe, A. M. and Bobinson B. H. (1987)J. Chem. Soc. Faraday Trans.1 83, Obinger, C., Maj, M., Nicholls, P. and Loewen, P. (1997) Arch. Biochem. Biophys. 342, G~bicka, L. and Pawlak, J. (1997) J. Mol. Catal. B 2,
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