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Electrical communication between horse heart cytochrome c and electrodes in the presence of DNA or RNA
179
J. Electroanal.
Chem., 287 (1990) 179-184
Elsevier Sequoia S.A., Lausarme - Printed in The Netherlands
Preliminary note
Electrical communication between horse heart cytochrome c and electrodes in the presence of DNA or RNA Osamu Ikeda *, Yukihiro Shirota and Takeshi Sakurai Department
of Chemistry,
College of Liberal Arts, Kanazawa
University,
I-I Marunouchi,
Kanazawa
920
(Japan) (Received 8 May 1990)
INTRODUCTION
Electrical communication between electrodes and enzymes has received active interest from the viewpoints of the clarification of electron transport mechanisms in biological systems, and of applications to biochemical sensors and biocatalyst electrodes. As has been reviewed by Armstrong et al. [l], direct electron exchange between electrodes and cytochrome c, one of the electron transport enzymes in mitochondria, has been successfully investigated by using metal oxide electrodes like In,O, [2], and promotors such as 4,4’-bipyridyl [3], dithiobis(ethanoic acid) [4], and bis(4-pyridyl)disulfide [5]. A feature common to the above promotors is that electron-rich nitrogen atoms or anions, which are able to interact with positively charged lysine residues in cytochrome c, are present at several tenths of a nm apart from electrode surfaces at the adsorbed state. We chose DNA or RNA and studied their suitability as a promotor, because they have negative charges and are actually present in mitochondria. As a result, we discovered that DNA or RNA works as an effective promotor by interacting electrostatically with the positively charged patch of cytochrome c. EXPERIMENTAL
Cytochrome c from horse hearts (Sigma; Type III) was used in the present study. DNA and RNA were sodium salts from salmon testes (Sigma; Type III) and from yeast (Kohjin), respectively. Various ribonucleotides, such as 5’-adenylic acid (AMP),
?&%&II
correspondence should be addressed.
0022-0728/90/$03.50 0 1990 - Else&r Sequoia S.A.
180
5’-uridylic acid (UMP), 5’-guanylic acid (GMP) and 5’xytidylic acid (CMP), were sodium salts from yeast (Sigma). All the reagents were used without further purification. The cyclic voltammogram of cytochrome c was measured using a Bioanalytical System (BAS) CV-1B cyclic voltammetry unit at a sweep rate of 5 mV s-l. A glassy carbon disc electrode with a surface area of 0.07 cm2 was used as the working electrode. The electrode surface was polished with alumina powder (0.3 pm) just before the measurement and then washed in an ultrasonic bath for a few minutes to detach any alumina powder. A Pt wire and an Ag/AgCl were used as the counter and the reference electrode, respectively. Kinetic parameters for the reduction of oxidized cytochrome c were estimated from the normal pulse voltammogram [6] measured by using a Yanagimoto P-1100 Voltammetric Analyzer. All the measurements were carried out at room temperature (ca. 20 o C). RESULTS
AND
DISCUSSION
Figure 1 shows the cyclic voltammograms of cytochrome c at the glassy carbon electrode in the phosphate buffer solution (pH = 7.4) with and without DNA, and the cyclic voltammogram of DNA in the same phosphate buffer solution. The cyclic
-0.2
I
I
0
0.2
E I V (VS. AglAgCl)
Fig. 1. Cyclic voltammograms
of 0.2 mM horse heart cytochrome
c with (a) (-
) and without (b)
(. -. - .) DNA in 5 mM phosphate buffer solution @H = 7.4). (c) (. . . . . .) DNA in the absence of cytochrome c. The concentration of DNA is 0.2 mg ml-‘. surface area of 0.07 cm2; sweep rate, 5 mV s-l.
Working electrode,
glassy carbon disc with a
181
Fig. 2. Dependence of AEp on the wnc~~ati~n of DNA (c DNA). Conditions cyclic voltammograms are the same as in Fig. 1.
for the measurement
of
voltammogram of cytochrome c in the absence of DNA showed an unstable irreversible wave. Thus anodic and cathodic currents decreased as the number of potential sweep cycles increased. Such instability of the cyclic voltammogram may be ascribed to the denat~ation of cytoc~ome c owing to contact adsorption [7]. On the other hand, the cyclic volt~o~~ in the presence of DNA was very stable and showed a quasi-reversible wave. The cyclic voltammogram showed no appreciable change even after 100 potential sweep cycles (5.6 h). Since no clear redox wave was observed in the cyclic voltammogram of DNA itself, DNA is considered to act not as a mediator but as a promotor in an el~tr~he~c~ sense. Almost the same results were also obtained for RNA. Discussions for DNA seem to hold also for RNA. Figure 2 shows the dependence of AEr, the difference between the anodic peak potential (Er,) and the cathodic peak potential (E,,), on the concentration of DNA (cuNA). It is well known that the AE, for a one-electron reversible system is 58 mV and it becomes larger with slowing down of the charge transfer rate [S]. When coNA is below 0.02 mg ml-i, the effect of DNA on the charge transfer is scarcely observable, but it becomes visible above 0.04 mg ml-i. The A& showed a minimum value at cDNA around 0.3 mg ml-‘, and again increased with an increase in coNA- The AEr at cur+, of 0.2 and 0.4 mg ml-’ was 63 and 60 mV, respectively, indicating a one-electron quasi-reversible process. The change of AE, shown in Fig_ 2 is considered to be due to the change in the amount of DNA adsorbed on the electrode surface. Thus, the electrode surface is suggested to be saturated with DNA at cDNA around 0.3 mg ml-*, which value is in good agreement with the value of about 0.2 mg ml -’ found by Miller for the positively charged mercury electrode [9]. This agreement may result from the somewhat similar potential of zero charge ( EpzC) for the glassy carbon and the mercury electrode, namely - 0.193 V vs. SHE for mercury [lo] and ca. 0 V vs. SHE for glassy carbon which was estimated from the double-layer capacitance for various carbon and graphite electrodes [11-131. This means that the electrode surface of glassy carbon is positively charged in the whole potential sweep range in Fig. 1. It was reported that double stranded nucleic
182 TABLE 1 Kinetic parameters for the reduction of oxidized cytochrome c in the presence of DNA or RNA Kinetic parameters
DNAa
RNA8
Literature value
E o ’ V (vs. SHE)
0.257 9.0
0.247 9.5
0.257 kO.017 [2] 8.9 (20 o C) [18] ll(25Oc.z) [2]
1.5
1.2
10’
D0
ci2 s-’ b ’
10s Pcm s-r b
a cDNA= caNA = 0.2 mg ml-‘. b Temperature at the measurement, 20*l°C. Concentration of cytochrome c, 0.2 mM in 5 n&i phosphate buffer solution @H = 7.4); working electrode, glassy carbon disc; potential sweep rate, 5 mV s-l; sampling time, 33.3 ms.
acids were adsorbed at the positively charged silver electrode [14,15]. In this sense, it seems most likely that DNA or RNA adsorbed on the positively charged electrode surface acts as an effective promotor for the electron transfer between electrode and cytochrome c. In fact, an Au electrode whose E,, is 0.19 V vs. SHE [16] showed no quasi-reversible wave in the cyclic voltammogram of cytochrome c in the presence of DNA or RNA, but an Ag electrode whose Epu: is -0.44 V vs. SHE [17] gave a quasi-reversible wave. The retardation of the electrical communication between the glassy carbon and cytochrome c, which was observed for cm+, over 0.4 mg ml-‘, may result from multi-layered adsorption of DNA. Table 1 summarizes the kinetic parameters for the reduction of oxidized cytochrome c. The formal potentials (E O’) of cytochrome c in the presence of DNA or RNA, which were evaluated as the mean of Epa and E,,, were 257 and 247 mV vs. SHE, respectively, and were very close to the potentiometric value [2]. The diffusion coefficients (D,) were also almost the same as the values in the literature [2,18]. Further, no specific change was observed in the absorption and circular dichroism spectra of the binary system containing cytochrome c and DNA or RNA. All the above results suggest that a strong interaction, which would give a structural deformation is not present between cytochrome c and DNA or RNA. Cytochrome c has many lysine residues, which are positively charged in a neutral solution. There are four uncompensated positive charges originating from Lys 25, 27, 72 and 79 on the front face of cytochrome c with a heme pocket. This face has been reported to be an entrance and an exit for electrons [19]. On the other hand, DNA is virtually an insulator, but a notable charge transfer from sugar to base has been suggested [20]. Therefore, electron transfer through DNA, if possible, seems to occur in the direction across the helix. In fact, it has been reported that the photoinduced electron transfer rate is accelerated by the presence of DNA [21-231. The electrical communication between electrodes and cytochrome c in the presence of DNA or RNA is ascribed to (i) a surface condensation of cytochrome c by nucleic acids or (ii) a fast electrical conduction through the base pair. In order to clarify which is more likely, the cyclic voltammogram of cytochrome c in various
183
I
I
I 0
-0.2 E / V
I
I
0.2
(VS.p;9IA9Cl)
Fig. 3. Cyclic voltammograms of 0.2 mM horse heart cytochrome c in various systems: (a) (e-.-.) 0.4 mg ml-’ sodium polyphosphate in 5 mM phosphate buffer (PH = 7.4); (b) (- - -) 5 mM 5’-cytidylic 2.5 acid sodium salt (CMP); (c) ( . . . . . .) 5 mM 5’-guanylic acid sodium salt (GMP); and (d) ( -) mM CMP + 2.5 mM GMP. Conditions for the measurement of cyclic voltammograms are the same as in Fig. 1.
systems was measured, and a part of the results is shown in Fig. 3. The cyclic voltammogram in the solution containing sodium polyphophate (Sigma; Type 75 + : average chain length 2 75 P) in place of DNA (curve a) showed AEp of 150 mV, suggesting that (i) is not a main factor. Curves (b) and (c) show the cyclic voltammogram in the solution of CMP and GMP, respectively. Unstable cyclic voltammograms similar to the one in the phosphate buffer solution were also obtained for the other ribonucleotides (AMP and CMP). Curve (d) is that in the solution containing an equimolar mixture of CMP and GMP. The cyclic voltammogram was stable and gave a AEp of 90 mV. However, no other possible combination of two ribonucleotides gave a cyclic voltammogram with such good reversibility as that for the combination of CMP and GMP. The results with respect to single ribonucleotides seem to be associated with the observation that ribonucleotides are adsorbed with the base moiety flat on the electrode surface [24,25], and such an orientation might not contribute to a fast electron transfer through the aromatic ring. On the other hand, the results with respect to the combination of two ribonucleotides seem to be associated with the fact that the base pair formation is the most feasible with the combination of CMP and GMP [26,27]. We speculate now that the base pair interacting electrostatically with cytochrome c makes a pathway for electrical communication between electrode and cytochrome c by orienting the aromatic ring vertically on the electrode surface.
184
When a double stranded DNA molecule is adsorbed in such a way that the helical axis becomes parallel to the electrode surface, the base pairs are vertically oriented against the electrode surface [28]. In that case, the distance between the electrode surface and the front face of cytochrome c is about 2 nm. Electrical communication in such a configuration may occur through hopping conduction through electrode/base p~r/cyt~~ome c. ACKNOWLEDGEMENT
We are grateful to Dr. N. Sugimoto of Kohnan suggestion about the base pair formation.
University
for his useful
REFERENCES 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28
F.A. Armstrong H.A.O. Hi and N.J. Walton, Act. Chem. Res., 21 (1988) 407. P. Yeh and T, Kuwana, Chem. Lett., (1977) 1145. M.J. Eddows and H.A.O. W, J. Chem. Sot., Chem. Commun., (1977) 771. P.M. Allen, H.A.O. Hill and N.J. Walton, J. Electroanal. Chem., 178 (1984) 69. I. Taniguchi, K. Toyosawa, H. Yama8uchi and K. Yasukouchi, J. Chem. Sot., Chem. Commun., (1982) 1032. B. Workie and T. Solomon, J. Ekxtroanal Chem., 224 (1987) 49. I. Taniguchi, Denki Kagaku, 56 (1988) 158. R.S. Nicholson, Anal. Chem., 37 (1965) 1351. LR. Miller, J. Mol. Biol., 3 (1961) 229. D. Grahame, Chem. Rev., 41(1947) 441. J.-P. Randin and E. Yeager, J. Electroaual. Chem., 36 (1972) 257. J.-P. Randin and E. Yeager, J. Electroam& Chem., 51 (1975) 313. J.-P. Randin iu A.J. Bard (Ed.), Encyclopedia of Electrochemistry of the Elements, Vol. 7, Marcel Dekker, New York, 1976, p. 36. K.H. Erwin, E. Koglin, J.-M. Sequaris, P. Valenta and H.W. Ntimberg, J. Electroanal. Chem., 114 (1980) 179. E. Koghn and J.-M. Sequaris, Top. Curr. Chem., 134 (1986) 1. J. Claviher and Nguyen vau Huong, C.R. Acad. Sci., Ser. C, 269 (1968) 5133. JG’M. Bockris, SD. Argade and E. Gileadi, Electrocbim. Acta, 14 (1969) 1259. R.C. Long, F.M. Hawkridge, J.F. Chlebowski and C.R. Hartzell, J. Electroaual. Cbem., 256 (1988) 111. P.L. Drake, R.T. Ha&shorn, J. McGiunis and A.G. Sykes, Inorg. Chem., 28 (1989) 1361. P. Otto, E. Clementi and 3. Ladik, J. Chem. Phys., 78 (1983) 4547. P. Fromherz and B. Rieger, J. Am. Chem. Sot., 108 (1986) 5361. J.K. Barton, C.V. Kumar and N.J. Turro, J. Am. Chem. Sot., 108 (1986) 6391. M.D. Purug8anaxx, C.V. Kumar, N.J. Turro and J.K. Barton, Science (Washington DC), 241 (1988) 1645. V. Brabec and K. Niki, Biophys. Chem., 23 (1985) 63. V. Brabec and K. Niki, Collect. Czech. Chem. Commun., 51 (1986) 167. S.M. Freier, R. Kierzek, J.A. Jaeger, N. Sugimoto, M.H. Caruthers, T. NeiIson and D.H. Turner, Proc. Natl. Acad. Sci. USA, 83 (1986) 9373. L. Katz and S. Penman, J. Mol. Biol., 15 (1966) 220. M.W. Humphreys and R. Parsons, J. EIectroauaI. Chem., 75 (1977) 427.
J. Electroanal.
Chem., 287 (1990) 179-184
Elsevier Sequoia S.A., Lausarme - Printed in The Netherlands
Preliminary note
Electrical communication between horse heart cytochrome c and electrodes in the presence of DNA or RNA Osamu Ikeda *, Yukihiro Shirota and Takeshi Sakurai Department
of Chemistry,
College of Liberal Arts, Kanazawa
University,
I-I Marunouchi,
Kanazawa
920
(Japan) (Received 8 May 1990)
INTRODUCTION
Electrical communication between electrodes and enzymes has received active interest from the viewpoints of the clarification of electron transport mechanisms in biological systems, and of applications to biochemical sensors and biocatalyst electrodes. As has been reviewed by Armstrong et al. [l], direct electron exchange between electrodes and cytochrome c, one of the electron transport enzymes in mitochondria, has been successfully investigated by using metal oxide electrodes like In,O, [2], and promotors such as 4,4’-bipyridyl [3], dithiobis(ethanoic acid) [4], and bis(4-pyridyl)disulfide [5]. A feature common to the above promotors is that electron-rich nitrogen atoms or anions, which are able to interact with positively charged lysine residues in cytochrome c, are present at several tenths of a nm apart from electrode surfaces at the adsorbed state. We chose DNA or RNA and studied their suitability as a promotor, because they have negative charges and are actually present in mitochondria. As a result, we discovered that DNA or RNA works as an effective promotor by interacting electrostatically with the positively charged patch of cytochrome c. EXPERIMENTAL
Cytochrome c from horse hearts (Sigma; Type III) was used in the present study. DNA and RNA were sodium salts from salmon testes (Sigma; Type III) and from yeast (Kohjin), respectively. Various ribonucleotides, such as 5’-adenylic acid (AMP),
?&%&II
correspondence should be addressed.
0022-0728/90/$03.50 0 1990 - Else&r Sequoia S.A.
180
5’-uridylic acid (UMP), 5’-guanylic acid (GMP) and 5’xytidylic acid (CMP), were sodium salts from yeast (Sigma). All the reagents were used without further purification. The cyclic voltammogram of cytochrome c was measured using a Bioanalytical System (BAS) CV-1B cyclic voltammetry unit at a sweep rate of 5 mV s-l. A glassy carbon disc electrode with a surface area of 0.07 cm2 was used as the working electrode. The electrode surface was polished with alumina powder (0.3 pm) just before the measurement and then washed in an ultrasonic bath for a few minutes to detach any alumina powder. A Pt wire and an Ag/AgCl were used as the counter and the reference electrode, respectively. Kinetic parameters for the reduction of oxidized cytochrome c were estimated from the normal pulse voltammogram [6] measured by using a Yanagimoto P-1100 Voltammetric Analyzer. All the measurements were carried out at room temperature (ca. 20 o C). RESULTS
AND
DISCUSSION
Figure 1 shows the cyclic voltammograms of cytochrome c at the glassy carbon electrode in the phosphate buffer solution (pH = 7.4) with and without DNA, and the cyclic voltammogram of DNA in the same phosphate buffer solution. The cyclic
-0.2
I
I
0
0.2
E I V (VS. AglAgCl)
Fig. 1. Cyclic voltammograms
of 0.2 mM horse heart cytochrome
c with (a) (-
) and without (b)
(. -. - .) DNA in 5 mM phosphate buffer solution @H = 7.4). (c) (. . . . . .) DNA in the absence of cytochrome c. The concentration of DNA is 0.2 mg ml-‘. surface area of 0.07 cm2; sweep rate, 5 mV s-l.
Working electrode,
glassy carbon disc with a
181
Fig. 2. Dependence of AEp on the wnc~~ati~n of DNA (c DNA). Conditions cyclic voltammograms are the same as in Fig. 1.
for the measurement
of
voltammogram of cytochrome c in the absence of DNA showed an unstable irreversible wave. Thus anodic and cathodic currents decreased as the number of potential sweep cycles increased. Such instability of the cyclic voltammogram may be ascribed to the denat~ation of cytoc~ome c owing to contact adsorption [7]. On the other hand, the cyclic volt~o~~ in the presence of DNA was very stable and showed a quasi-reversible wave. The cyclic voltammogram showed no appreciable change even after 100 potential sweep cycles (5.6 h). Since no clear redox wave was observed in the cyclic voltammogram of DNA itself, DNA is considered to act not as a mediator but as a promotor in an el~tr~he~c~ sense. Almost the same results were also obtained for RNA. Discussions for DNA seem to hold also for RNA. Figure 2 shows the dependence of AEr, the difference between the anodic peak potential (Er,) and the cathodic peak potential (E,,), on the concentration of DNA (cuNA). It is well known that the AE, for a one-electron reversible system is 58 mV and it becomes larger with slowing down of the charge transfer rate [S]. When coNA is below 0.02 mg ml-i, the effect of DNA on the charge transfer is scarcely observable, but it becomes visible above 0.04 mg ml-i. The A& showed a minimum value at cDNA around 0.3 mg ml-‘, and again increased with an increase in coNA- The AEr at cur+, of 0.2 and 0.4 mg ml-’ was 63 and 60 mV, respectively, indicating a one-electron quasi-reversible process. The change of AE, shown in Fig_ 2 is considered to be due to the change in the amount of DNA adsorbed on the electrode surface. Thus, the electrode surface is suggested to be saturated with DNA at cDNA around 0.3 mg ml-*, which value is in good agreement with the value of about 0.2 mg ml -’ found by Miller for the positively charged mercury electrode [9]. This agreement may result from the somewhat similar potential of zero charge ( EpzC) for the glassy carbon and the mercury electrode, namely - 0.193 V vs. SHE for mercury [lo] and ca. 0 V vs. SHE for glassy carbon which was estimated from the double-layer capacitance for various carbon and graphite electrodes [11-131. This means that the electrode surface of glassy carbon is positively charged in the whole potential sweep range in Fig. 1. It was reported that double stranded nucleic
182 TABLE 1 Kinetic parameters for the reduction of oxidized cytochrome c in the presence of DNA or RNA Kinetic parameters
DNAa
RNA8
Literature value
E o ’ V (vs. SHE)
0.257 9.0
0.247 9.5
0.257 kO.017 [2] 8.9 (20 o C) [18] ll(25Oc.z) [2]
1.5
1.2
10’
D0
ci2 s-’ b ’
10s Pcm s-r b
a cDNA= caNA = 0.2 mg ml-‘. b Temperature at the measurement, 20*l°C. Concentration of cytochrome c, 0.2 mM in 5 n&i phosphate buffer solution @H = 7.4); working electrode, glassy carbon disc; potential sweep rate, 5 mV s-l; sampling time, 33.3 ms.
acids were adsorbed at the positively charged silver electrode [14,15]. In this sense, it seems most likely that DNA or RNA adsorbed on the positively charged electrode surface acts as an effective promotor for the electron transfer between electrode and cytochrome c. In fact, an Au electrode whose E,, is 0.19 V vs. SHE [16] showed no quasi-reversible wave in the cyclic voltammogram of cytochrome c in the presence of DNA or RNA, but an Ag electrode whose Epu: is -0.44 V vs. SHE [17] gave a quasi-reversible wave. The retardation of the electrical communication between the glassy carbon and cytochrome c, which was observed for cm+, over 0.4 mg ml-‘, may result from multi-layered adsorption of DNA. Table 1 summarizes the kinetic parameters for the reduction of oxidized cytochrome c. The formal potentials (E O’) of cytochrome c in the presence of DNA or RNA, which were evaluated as the mean of Epa and E,,, were 257 and 247 mV vs. SHE, respectively, and were very close to the potentiometric value [2]. The diffusion coefficients (D,) were also almost the same as the values in the literature [2,18]. Further, no specific change was observed in the absorption and circular dichroism spectra of the binary system containing cytochrome c and DNA or RNA. All the above results suggest that a strong interaction, which would give a structural deformation is not present between cytochrome c and DNA or RNA. Cytochrome c has many lysine residues, which are positively charged in a neutral solution. There are four uncompensated positive charges originating from Lys 25, 27, 72 and 79 on the front face of cytochrome c with a heme pocket. This face has been reported to be an entrance and an exit for electrons [19]. On the other hand, DNA is virtually an insulator, but a notable charge transfer from sugar to base has been suggested [20]. Therefore, electron transfer through DNA, if possible, seems to occur in the direction across the helix. In fact, it has been reported that the photoinduced electron transfer rate is accelerated by the presence of DNA [21-231. The electrical communication between electrodes and cytochrome c in the presence of DNA or RNA is ascribed to (i) a surface condensation of cytochrome c by nucleic acids or (ii) a fast electrical conduction through the base pair. In order to clarify which is more likely, the cyclic voltammogram of cytochrome c in various
183
I
I
I 0
-0.2 E / V
I
I
0.2
(VS.p;9IA9Cl)
Fig. 3. Cyclic voltammograms of 0.2 mM horse heart cytochrome c in various systems: (a) (e-.-.) 0.4 mg ml-’ sodium polyphosphate in 5 mM phosphate buffer (PH = 7.4); (b) (- - -) 5 mM 5’-cytidylic 2.5 acid sodium salt (CMP); (c) ( . . . . . .) 5 mM 5’-guanylic acid sodium salt (GMP); and (d) ( -) mM CMP + 2.5 mM GMP. Conditions for the measurement of cyclic voltammograms are the same as in Fig. 1.
systems was measured, and a part of the results is shown in Fig. 3. The cyclic voltammogram in the solution containing sodium polyphophate (Sigma; Type 75 + : average chain length 2 75 P) in place of DNA (curve a) showed AEp of 150 mV, suggesting that (i) is not a main factor. Curves (b) and (c) show the cyclic voltammogram in the solution of CMP and GMP, respectively. Unstable cyclic voltammograms similar to the one in the phosphate buffer solution were also obtained for the other ribonucleotides (AMP and CMP). Curve (d) is that in the solution containing an equimolar mixture of CMP and GMP. The cyclic voltammogram was stable and gave a AEp of 90 mV. However, no other possible combination of two ribonucleotides gave a cyclic voltammogram with such good reversibility as that for the combination of CMP and GMP. The results with respect to single ribonucleotides seem to be associated with the observation that ribonucleotides are adsorbed with the base moiety flat on the electrode surface [24,25], and such an orientation might not contribute to a fast electron transfer through the aromatic ring. On the other hand, the results with respect to the combination of two ribonucleotides seem to be associated with the fact that the base pair formation is the most feasible with the combination of CMP and GMP [26,27]. We speculate now that the base pair interacting electrostatically with cytochrome c makes a pathway for electrical communication between electrode and cytochrome c by orienting the aromatic ring vertically on the electrode surface.
184
When a double stranded DNA molecule is adsorbed in such a way that the helical axis becomes parallel to the electrode surface, the base pairs are vertically oriented against the electrode surface [28]. In that case, the distance between the electrode surface and the front face of cytochrome c is about 2 nm. Electrical communication in such a configuration may occur through hopping conduction through electrode/base p~r/cyt~~ome c. ACKNOWLEDGEMENT
We are grateful to Dr. N. Sugimoto of Kohnan suggestion about the base pair formation.
University
for his useful
REFERENCES 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28
F.A. Armstrong H.A.O. Hi and N.J. Walton, Act. Chem. Res., 21 (1988) 407. P. Yeh and T, Kuwana, Chem. Lett., (1977) 1145. M.J. Eddows and H.A.O. W, J. Chem. Sot., Chem. Commun., (1977) 771. P.M. Allen, H.A.O. Hill and N.J. Walton, J. Electroanal. Chem., 178 (1984) 69. I. Taniguchi, K. Toyosawa, H. Yama8uchi and K. Yasukouchi, J. Chem. Sot., Chem. Commun., (1982) 1032. B. Workie and T. Solomon, J. Ekxtroanal Chem., 224 (1987) 49. I. Taniguchi, Denki Kagaku, 56 (1988) 158. R.S. Nicholson, Anal. Chem., 37 (1965) 1351. LR. Miller, J. Mol. Biol., 3 (1961) 229. D. Grahame, Chem. Rev., 41(1947) 441. J.-P. Randin and E. Yeager, J. Electroaual. Chem., 36 (1972) 257. J.-P. Randin and E. Yeager, J. Electroam& Chem., 51 (1975) 313. J.-P. Randin iu A.J. Bard (Ed.), Encyclopedia of Electrochemistry of the Elements, Vol. 7, Marcel Dekker, New York, 1976, p. 36. K.H. Erwin, E. Koglin, J.-M. Sequaris, P. Valenta and H.W. Ntimberg, J. Electroanal. Chem., 114 (1980) 179. E. Koghn and J.-M. Sequaris, Top. Curr. Chem., 134 (1986) 1. J. Claviher and Nguyen vau Huong, C.R. Acad. Sci., Ser. C, 269 (1968) 5133. JG’M. Bockris, SD. Argade and E. Gileadi, Electrocbim. Acta, 14 (1969) 1259. R.C. Long, F.M. Hawkridge, J.F. Chlebowski and C.R. Hartzell, J. Electroaual. Cbem., 256 (1988) 111. P.L. Drake, R.T. Ha&shorn, J. McGiunis and A.G. Sykes, Inorg. Chem., 28 (1989) 1361. P. Otto, E. Clementi and 3. Ladik, J. Chem. Phys., 78 (1983) 4547. P. Fromherz and B. Rieger, J. Am. Chem. Sot., 108 (1986) 5361. J.K. Barton, C.V. Kumar and N.J. Turro, J. Am. Chem. Sot., 108 (1986) 6391. M.D. Purug8anaxx, C.V. Kumar, N.J. Turro and J.K. Barton, Science (Washington DC), 241 (1988) 1645. V. Brabec and K. Niki, Biophys. Chem., 23 (1985) 63. V. Brabec and K. Niki, Collect. Czech. Chem. Commun., 51 (1986) 167. S.M. Freier, R. Kierzek, J.A. Jaeger, N. Sugimoto, M.H. Caruthers, T. NeiIson and D.H. Turner, Proc. Natl. Acad. Sci. USA, 83 (1986) 9373. L. Katz and S. Penman, J. Mol. Biol., 15 (1966) 220. M.W. Humphreys and R. Parsons, J. EIectroauaI. Chem., 75 (1977) 427.