Reduction of p-benzoquinone on lipid-modified electrodes: effect of the alkyl chain length of lipids on the electron transfer reactions
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1 Journal of Electroanalytical Chemistry 484 (2000) Reduction of p-benzoquinone on lipid-modified electrodes: effect of the alkyl chain length of lipids on the electron transfer reactions Hyun Park a,b, Munetaka Oyama a, Yoon-Bo Shim b, Satoshi Okazaki a, * a Department of Material Chemistry, Graduate School of Engineering, Kyoto Uni ersity, Yoshida, Sakyo-ku, Kyoto , Japan b Department of Chemistry, Pusan National Uni ersity, Pusan , South Korea Received 2 March 1999; received in revised form 14 January 2000; accepted 26 January 2000 Abstract Using a phosphatidylcholine (PC) modified electrode, an unusual stabilization of p-benzoquinone anion radical (BQ )is observed even in a buffered solution of ph 7.0. To clarify this incorporation reaction of BQ in a PC layer, the effect of the molecular structure of the lipid was studied by constructing the PC modified electrodes with four PC derivatives; dicaproyl-, dilauroyl-, dipalmitoyl- and diarachidoyl-pc. At 25 C, dilauroyl-pc with a moderate alkyl chain length stabilized BQ and allowed the approach of benzoquinol onto the surface of the modified electrode. From the ph dependence of the electrochemical responses, the incorporation mechanism of BQ with P(O)OH was clarified. In addition to dilauroyl-pc, because dipalmitoyl- PC was found to incorporate BQ over 40 C, the relationship between its incorporation and the phase transition temperature of each lipid has become clear. The correlation and the incorporation profiles were examined by measuring the oxidation of benzoquinol as well as that of BQ. Also, the diffusion coefficients were determined for the lipids incorporating BQ Elsevier Science S.A. All rights reserved. Keywords: Reduction of benzoquinone; Benzoquinone anion radical; Lipid modified electrode; Alkyl chain length of lipid; Phase transition temperature of lipid 1. Introduction Studies on the electron transfer reactions of a lipidmodified electrode provide useful information for elucidating biological electron transfer processes concerning lipid layers. In a previous paper [1], we reported that a reduction product of p-benzoquinone (BQ), the BQ anion radical ( ), was incorporated into an eggphosphatidylcholine (PC) modified electrode through the interaction between and a phosphate group, P(O)OH, in a hydrated PC molecule. While the chemistry of BQ has been studied extensively [2 8], the results obtained using the PC coated electrode exhibited an unusual stabilization even in a buffered solution of ph 7.0. It could be concluded that this was * Corresponding author. Tel.: ; fax: address: okazaki@mc.kyoto-u.ac.jp (S. Okazaki) strongly related to the hydrophobic nature of the PC layers as well as to the formation of hydrogen bonding between and P(O)OH. No significant effect of N(CH 3 ) 3+ in the head group (called choline) was observed when was incorporated as was shown by the electrochemical responses of phophatidic acid (PA) [1]. Thus, in order to elucidate the structural effect of lipids on the electron transfers of BQ, it is preferable to examine the effect of the tail group, i.e. the effect of the alkyl chain length of the lipid. Because the tail group governs, in particular, the hydrophobic nature of the lipid, the interaction between the lipid and BQ or would vary depending on the different tail group. Because the egg PC used in the previous study [1] contained various lengths of R 1 and R 2, measurement using lipids having defined alkyl chains would be effective in clarifying the interactions. In the present work, we used electrodes modified with the pure PC derivatives to investigate the relationship between the electron /00/$ - see front matter 2000 Elsevier Science S.A. All rights reserved. PII: S (00)00067-X
2 132 H. Park et al. / Journal of Electroanalytical Chemistry 484 (2000) transfer reactions of BQ and the hydrophobic property of the various lipids. Four compounds, dicaproyl-pc (n=6 inr 1 and R 2 ), dilauroyl-pc (n=12), dipalmitoyl-pc (n=16) and diarachidoyl-pc (n=20), were selected based on the differences in their alkyl chain lengths. The hydrophobic property is assumed to be enhanced with the increase of the alkyl chain length. The electrochemical behavior of BQ, in particular, the incorporation, depending on the changes in the hydrophobic property was examined using electrodes modified with these four lipids. In addition, the ph and temperature effects on the reactions were also analyzed in detail Procedures and equipment The glassy carbon (GC, Tokay Carbon Co., GC-20S) disk (diameter; 0.3 mm) electrode was modified by the method described in Ref. [1] and then we determined the thickness and area of the lipid layer using SEM. All potentials were measured and are reported versus Ag AgCl (sat. KCl). The counter electrode was a Pt wire. A thermostat (TAITEC (Dx-100)) was used to control the temperature of the sample solution. Electrochemical measurements were carried out using HUSO electrochemical systems, HUSO 980 and HUSO 311B, and a GRAPHTEC XY recorder, WX Experimental 2.1. Materials p-benzoquinone (BQ, Nacalai Tesque, GR grade) was purified by sublimation under a reduced pressure. Phosphatidylcholine derivatives, dicaproyl-pc (Sigma), dilauroyl-pc (Wako), dipalmitoyl-pc (Wako), and diarachidoyl-pc (Sigma) were used without further purification. All lipids solutions used for coating electrodes were prepared daily as chloroform solutions of M lipid. The phosphate buffer solutions (Na 2 HPO 4 +NaH 2 PO 4 ) prepared from commercial GR grade reagents. The ph of these buffers was measured before and after experiments. Fig. 1. Cyclic voltammograms of BQ in a phosphate buffer with bare (a) and lipid modified electrodes (b e) at 25 C. Lipid; (b) dicaproyl- PC (n=6); (c) dilauroyl-pc (n=12); (d) dipalmitoyl-pc (n=16); and (e) diarchidoyl-pc (n=20). Scan rate, 20 mv s 1. [BQ], 1.0 mm. ph 7.0. Before measurement, the potential was held at 0.6 V for 15 min. 3. Results and discussion 3.1. Electrochemical responses depending on lipid chain length Fig. 1 shows cyclic voltammograms (CVs) recorded for 1.0 mm BQ in a 0.1 M phosphate buffer solution (ph 7.0) using a bare GC electrode and the lipid modified electrode at 25 C. All CVs were obtained after the applied potential was held at 0.6 V for 15 min to examine the reductive incorporation. With the bare GC electrode, BQ is reduced to hydroquinone (benzoquinol, BQH 2 ) in aqueous solution, not forming, as described by the following equation. BQ+2e +2H + BQH 2 (1) The redox waves of BQ to BQH 2 were observed, as shown in Fig. 1a, where the peaks I a and I c denote the oxidation peak of BQH 2 and the reduction peak of BQ, respectively. On the other hand, for the lipid modified electrodes, the electrochemical responses changed depending on the alkyl chain length, and the electrodes were classified into the following three groups according to their responses. The first group was the dicaproyl-pc (n=6) modified electrode, which showed the same CV patterns ( / V) as the bare GC electrodes as shown in Fig. 1b. This means that was not stabilized in the lipid layer composed of the PC having a short alkyl chain length. As mentioned before, the hydrophobic property of lipids is controlled by the nature of the tail group. Also, the egg-pc stabilized the anion radical even in the aqueous solution. Thus, from this result (Fig. 1b), it can be inferred that there is no stabilization effect in the less hydrophobic lipid layer, and that BQH 2 is formed and oxidized on the electrode surfaces as in the case of the bare GC electrode.
3 H. Park et al. / Journal of Electroanalytical Chemistry 484 (2000) extent by the surface of the modified electrode, using the longer alkyl chain lipid due to the increased rigidity. It is also probable that the resistance on the modified electrode surface increases due to the relatively high hydrophobic character and poor conductivity of the lipids, which will hinder the electron transfer reactions, compared with the GC electrode Thus, from the CV measurement of the lipids with the different chain lengths, we can conclude that the lipids having a medium number of the alkyl chain in the tail properly stabilize and allow the electron transfer reactions in aqueous media Dependence of the incorporation with dilauroyl-pc on ph Fig. 2. Changes in (E pa +E pc )/2 of peak I, I, and II. (a) Dependence of (E pa +E pc )/2 ofi( ) with a bare GC electrode. (b) Dependence of (E pa +E pc )/2 ofi ( ) and II ( ) with a dilauroyl-pc (n=12) modified electrode. The second group was the dilauroyl-pc (n=12) modified electrode, which showed new redox peaks marked II a ( V) and II c ( V) in the CV as shown in Fig. 1c. In addition, these showed the oxidation peak of BQH 2 (I a, V) and the reduction peak of BQ (I c, V). Since this result is quite similar to that obtained using the egg-pc modified electrode in the previous paper [1], the new peaks (II a,ii c ) could be attributed to the redox waves. Under the conditions for this CV measurement, the current of the peak II a was higher than that of the peak I a. While the potential and height of the peak I c was quite similar to that of the CV obtained with the bare GC electrode, the peak I a was slightly different from the peak I a in Fig. 1a. The reasons for this difference will be discussed in the next section. The appearance of peaks II a and II c justified that this length of alkyl chain, CO(CH 2 ) 10 CH 3, properly stabilized and incorporated in the lipid layer. In addition, this electrode is assigned to allow the redox reaction of BQH 2, which could be confirmed from the appearance of peaks I a and I c. The third group included the dipalmitoyl-pc (n=16) and diarachidoyl (n=20) modified electrodes. The peak potentials were / V and / V using the dipalmitoyl-pc and diarachidoyl-pc electrodes, respectively. The height of the redox peaks concerning BQH 2 for these electrodes was decreased to ca. 1/5 compared with that of the bare electrode. From these results, it is inferred that the penetration of redox species into the lipid layer was further hindered to some To examine the redox behavior of the dilauroyl-pc (n=12) modified electrode in more detail, we observed the relationship between ph and the peak potentials of and peak I in an aqueous buffer solution. In the ph region of 2 9, the oxidation/reduction peak of was observed with the dilauroyl-pc (n=12) modified electrode. Fig. 2 shows a plot of ph versus (E pa +E pc )/2 of peaks I, I and II. With the bare GC electrode, the potential shift of (E pa,i +E pc,i )/2 depending on ph had a slope of 60 mv ph 1, which was in accordance with Eq. (1). In contrast, with the lipid modified electrode, as shown in Fig. 2, the slope was 39 mv ph 1 when ph 4.0, whereas the slope reached 60 mv ph 1 when ph 4.0. The value less than 60 mv ph 1 implies strongly the existence of the following equation, BQ+2e +H + BQH (2) because, on the basis of this equation, the slope should be 30 mv ph 1. Therefore, by taking into account Eqs. (1) and (2) and the value of the slope obtained, it is inferred that the lipid layer accumulated H + by forming the hydrated phosphate form ( P(O)OH), which was favorable to the incorporation, and prevented the further approach of H + in the lipid layer. The insufficiency of H + ions within the Nernst diffusion region of the lipid modified electrode leads to the co-existence of two equilibria, Eqs. (1) and (2), which should cause the anion radical value of the slope. The constant potential value of peak II not depending on ph would be sound evidence that the reaction is attributed to the oxidation as expressed by Eq. (3), in addition to the previous result of the UV vis measurement [1]. In addition, Moncelli et al. reported that the reduction of ubiquinone (UQ) to ubiquinol (UQH 2 ) in a self-assembled phospholipid monolayer takes place via the formation of the semiubiquinone anion radical (UQ. ) in the ph range from 7 to 9.5 range [9].
4 134 H. Park et al. / Journal of Electroanalytical Chemistry 484 (2000) BQ+e (3) 3.3. Relationship between electrochemical response and phase transition temperature Actually, many biological membranes mainly contain lipids having the tails CO(CH 2 ) 14 CH 3 or CO(CH 2 ) 16 CH 3. In order to explain the different behavior of dipalmitoyl-pc (n=16) from dilauroyl-pc (n=12), we measured the CVs for 1.0 mm BQ in a 0.1 M phosphate buffer solution (ph 7.0) using the GC electrode and the lipid modified electrodes at 45 C. Fig. 3. Cyclic voltammograms of BQ in a phosphate buffer with bare (a) and lipid modified electrodes (b e) at 45 C. Lipid; (b) dicaproyl- PC (n=6); (c) dilauroyl-pc (n=12); (d) dipalmitoyl-pc (n=16); and (e) diarchidoyl-pc (n=20). Scan rate, 20 mv s 1. [BQ], 1.0 mm. ph 7.0. Before measurement, the potential was held at 0.6 V for 15 min. Fig. 4. Dependence of the oxidation peak current of BQ (peak II a ) on the measurement temperature. Lipid; dilauroyl-pc (n=12) ( ) and dipalmitoyl-pc (n=16) ( ). Each lipid has a specific phase transition temperature (T c ). The T c of dilauroyl-pc (n=12) is 0 C, and that of dipalmitoyl-pc (n=16) is 42 C [10]. Hence, the measurement temperature of 45 C for CV is over the T c values for both lipids. Fig. 3 shows the observed CVs at 45 C. While the interpretations for the dicaproyl-pc (n=6) and diarachidoyl-pc (n=20) were similar to those in Fig. 1, a dramatic change was observed for the dipalmitoyl-pc (n=16) modified electrode, as is shown in Fig. 3d. That is, at 45 C, the redox peak appeared markedly in addition to the redox peak of BQH 2 and the current magnitude of the oxidation was higher than that observed for the dilauroyl-pc (n=12) modified electrode. This result indicates that the incorporation of depends significantly on the temperature as well as the kind of lipid used. From the results with the dilauroyl-pc (n=12) and the dipalmitoyl-pc (n=16) modified electrode, it is inferred that the incorporation is strongly related to the T c values. Below the T c, PCs exist in a highly ordered state with a rigid form, which is characterized as a solid-like phase called the gel [11]. An increase in temperature over T c causes the formation of gauche orientations, leading to kinks in the hydrocarbon chains and an increase in fluidity of the layer. This chain melting over T c results in the formation of a lamellar liquid crystal phase. The interpretation of the present results could be that while the dipalmitoyl-pc (n=16) could not incorporate at 25 C, it is presumed that the dipalmitoyl-pc obtained enough fluidity to stabilize over T c, i.e. at 45 C. Therefore, at this stage, we could conclude that the lipids having appropriate length of the alkyl chain in the tail group stabilize depending upon the temperature, in particular, the T c Temperature dependence incorporation To investigate the correlation between the incorporation and the T c in more detail, we observed the dependence of the oxidation of the incorporated at various temperatures using the lipid-modified electrodes. Fig. 4 shows the relationship between the peak current of the oxidation (II a ) and the measurement temperature for the dilauroyl-pc (n=12) and dipalmitoyl-pc (n=16) modified electrodes. For the dilauroyl-pc (n=12), for which the incorporation was observed both at 25 and 45 C, the incorporation was confirmed in the temperature range of C. The current maximum was observed at 30 C. In contrast, for dipalmitoyl-pc (n=16), for which the incorporation was observed at 45 C, and not at 25 C, the oxidation current of BQ was found to appear over 40 C, and the current maximum was at around 50 C.
5 H. Park et al. / Journal of Electroanalytical Chemistry 484 (2000) rating CV waves as indicated by the current values in Fig Temperature dependence of the oxidation peak potential of benzoquinol Fig. 5. Dependence of oxidation peak potentials of benzoquinol (peak I a and I a ) on the measurement temperature. (a) Bare GC electrode ( ) and (b) lipid modified electrode. Lipid, dilauroyl-pc (n=12) ( ) and dipalmitoyl-pc (n=16) ( ). Scan rate, 20 mv s 1. Another correlation with the T c was observed for the redox couple of BQ and benzoquinol (BQH 2 and BQH ) on the dilauroyl-pc (n=12) and dipalmitoyl- PC (n=16) modified electrodes. Fig. 5 shows the plot of the peak potential of I a and I a versus the measurement temperature. On the bare GC electrode, the peak potentials were shifted linearly to the negative potential depending on the temperature as shown in Fig. 5a. On the other hand, for the dilauroyl-pc (n=12) modified electrode, an almost linear shift was observed on the potential as shown in Fig. 5b ( ), but the slope was ca. six times that of the bare GC electrode. For the dipalmitoyl-pc (n=16) modified electrode, whereas, the slope was similar to that of the bare GC electrode below 40 C, the slope increased to over 40 C to reach the value observed for the dilauroyl-pc (n=12) modified electrode. These results strongly suggest the correlation between T c and the redox reaction of BQ and benzoquinol in the lipid layer. Over T c, the promotion of the oxidation of benzoquinol is expected with the increase of temperature as shown in the potential dependence in Fig Elucidation of the incorporation equilibrium of on the lipid layer Fig. 6. Changes in the peak current of oxidation of BQ (peak II a ) depending on holding time at 0.6 V with a dilauroyl-pc modified electrode. [BQ], 1.0 mm ( ), 3.0 mm ( ) and 5.0 mm ( ) in phosphate buffer, ph 7.0. From Fig. 4, it is suggested that the incorporation of BQ occurs at the appropriate temperature, which was greater than the phase transition temperature of the lipid. This is in contrast to the results that the redox peak current of BQH 2 increased linearly with an increase in temperature for the bare GC electrode (the result is not shown as a figure). The temperature for the incorporation maximum was higher than the T c of each lipid. A probable reason for this is that the system needed more energy to allow the interaction between the lipids and BQ than that required for merely changing the state of the lipids. Even at the high temperature of 60 C, the lipid layer on the surface was stable enough to show the incorpo- To examine the incorporated reaction in the lipid layer, we observed the dependence of the electrochemical responses on the BQ concentration in phosphate buffer (ph 7.0). As a result, using a dilauroyl-pc (n=12) modified electrode at 25 C, the slope of the CVs was almost the same for the solutions of 1.0 and 5.0 mm BQ, although the current value was different, after holding the potential at 0.6 V for 15 min. Because this implied that the reduction species of BQ in the reduction atmosphere in the lipid is in equilibrium, we also observed the effect of the holding time on the amount incorporated. Fig. 6 shows the plot of the peak current versus the holding time using a dilauroyl-pc (n=12) modified electrode for the solutions of 1.0, 3.0 and 5.0 mm BQ. In all cases, the peak currents increased with an increase of the holding time for 15 min, and reached plateau values when the holding time increased over 15 min. Furthermore, the total accumulated values were found to be dependent on the concentration of BQ in the buffer solution. Similar results were obtained with the dipalmitoyl-pc (n=16) modified electrode at 45 C.
6 136 H. Park et al. / Journal of Electroanalytical Chemistry 484 (2000) These results suggest that is captured by P(O)OH in the equilibrium as expressed by the following equation. P(O)OH P(O)OH+ (4) While the diffusion of H + into the lipid layer is expected to be disturbed by the increased hydrophobic nature of the lipid, the diffusion of BQ into the lipid layer should be allowed judging from the increased incorporation with time Diffusion coefficients in lipid layer To estimate the motion in the lipid layer, the diffusion coefficients were determined by using chronoamperometry and by analyzing with the Cottrell equation [12]. In this experiment, the electrode potential was stepped from 0.6 to 0.0 V to minimize the influence of the concurrent oxidation of benzoquinol. The diffusion coefficients (D o ) determined by a dilauroyl-pc coated electrode were and cm 2 s 1 at 25 and 45 C, respectively. The D values were calculated to be about 10 7 cm 2 s 1 at the other temperatures. The diffusion coefficient in the reduction of BQ was reported to be cm 2 s 1 [13]. Thus, the present result showed that the diffusion is suppressed in the lipid layers compared with that in an aqueous solution. Furthermore, from the result of the measurement of the dependence of D o on the temperature, the linear correlation was not observed with absolute temperature, T, although D o should be proportional to T by the Stokes Einstein equation. This phenomenon may be caused by the viscosity change of a lipid, which is also a temperature-dependent parameter. These results show that the diffusion coefficient of depends significantly on the state of the lipid caused by the increased temperature over T c as discussed above, not on the temperature itself. Thus, while the value for the dipalmitoyl-pc (n=16) modified electrodes was larger than that for the dilauroyl-pc (n= 12) electrode, the quantitative comparison seems to be difficult for determining the effect of the alkyl chain length of the diffusion. 4. Conclusions By using lipid modified electrodes having a defined alkyl chain length, the electrochemical behavior of BQ, in particular, the incorporation, was studied thoroughly in correlation with the hydrophobic property of the lipids and the measurement temperature. While the dicaproyl-pc, having a short chain length (n=6), did not stabilize BQ at all and the dipalmitoyl-pc (n=16) and diarachidoyl-pc (n=20) modified electrodes exhibited much lower redox currents for the BQ/BQH 2 couple at 25 C, the dilauroyl-pc (n=12) modified electrode stabilized and incorporated and permitted the approach of benzoquinol species into the lipid layer. Thus, it can be concluded that lipids having a medium n value of the alkyl chain in the tail allowed the electron transfer and benzoquinol. For the dilauroyl-pc (n=12) modified electrode, the ph dependence the oxidation peak potentials showed the existence of BQH as well as BQH 2. In addition, was incorporated into the dipalmitoyl-pc (n=16) modified electrode over 45 C; i.e. the incorporation was found to be correlated strongly with the phase transition temperature of each lipid. The differences between the dilauroyl-pc (n=12) and the dipalmitoyl-pc (n=16) modified electrodes depending on the measurement temperature could be evaluated from the electrochemical behavior of the redox reactions concerning BQ. For further evaluation of the lipid layer, which was found to have various influences of the redox reactions concerning BQ, studies using other surface analysis technique are now in progress. Acknowledgements This work was supported in part by a grant-in-aid for Scientific Research from the Ministry of Education, Science, Sports and Culture, Japan and by the Korea Science and Engineering Foundation ( ). H. Park is grateful for a the Japanese Government (Monbusho) scholarship as a research student in the Graduate School of Engineering, Kyoto University. References [1] H. Park, J.S. Park, Y.B. Shim, J. Electroanal. Chem. 438 (1997) 113. [2] R.A. Morton (Ed.), Biochemistry of Quinones, Wiley, New York, [3] J.M. Hale, R. Parsons, Trans. Faraday Soc. 59 (1963) [4] E. Zeigerson, E. Gileadi, J. Electroanal. Chem. 28 (1970) 421. [5] D.H. Evans, Chem. Rev. 90 (1990) 739. [6] S.I. Bailey, I.M. Ritchie, Electrochim. Acta 30 (1985) 3. [7] K.S.V. Santhanam, R.N. O Brien, J. Electroanal. Chem. 160 (1984) 377. [8] Y.B. Shim, S.M. Park, J. Electroanal. Chem. 425 (1997) 201. [9] (a) M.R. Moncelli, L. Becucci, A. Nelson, R. Guidelli, Biophys. J. 70 (1996) (b) M.R. Moncelli, R. Herrero, L. Becucci, R. Guidelli, Biochim. Biophys. Acta 1364 (1998) 373. [10] The Japanese Biochemical Society (Ed.), Lipid II: Phospholipid, Japan, 1991, p [11] A.G. Lee, Biochim. Biophys. Acta 472 (1977) 237. [12] A.J. Bard, L.R. Faulkner, Electrochemical Methods: Fundamentals and Applications, Wiley, New York, [13] R.N. Adams, Electrochemistry at Solid Electrodes, Marcel Dekker, New York, 1969.
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