ARTICLE pubs.acs.org/JPCB
Canolol: A Promising Chemical Agent against Oxidative Stress Annia Galano,*,† Misaela Francisco-Marquez,† and Juan R. Alvarez-Idaboy†,‡ Departamento de Quimica, Universidad Autonoma Metropolitana-Iztapalapa, San Rafael Atlixco 186, Col. Vicentina. Iztapalapa, C. P. 09340, Mexico D. F. Mexico ‡ Facultad de Quimica, Departamento de Fisica y Quimica Teorica, Universidad Nacional Autonoma de Mexico, Mexico DF 04510, Mexico †
bS Supporting Information ABSTRACT: The OOH radical scavenging activity of canolol (CNL) has been studied in aqueous and lipid solutions, using the density functional theory. CNL is predicted to react about 3.6 times faster in aqueous solution than in lipid media. The overall rate coefficients are predicted to be 2.5 106 and 6.8 105 M1 s1, respectively. The OOH radical scavenger activity of canolol is predicted to be similar to that of carotenes, higher than that of allicin, and much higher than that of melatonin. Branching ratios for the different channels of reaction are reported for the first time. It was found that the reactivity of canolol toward OOH radicals takes place almost exclusively by H atom transfer from the phenolic moiety in canolol, regardless of the polarity of the environment. Taking into account that the reactivity of peroxyl radicals is significantly lower than that of other reactive oxygen species, canolol is proposed to be a very good antioxidant.
’ INTRODUCTION Canolol (CNL), also known as vinylsyringol, has been recently isolated from crude canola oil and identified as a decarboxylation product of sinapinic acid.1,2 It is a phenolic compound, and this kind of compounds is known for scavenging free radicals.3 Koski et al.1 were the first to observe the antioxidant activity of CNL and reported that its lipid protective activity is similar to that of γ-tocopherol. Shortly after, Kuwahara et al.4 found that CNL reduces intracellular oxidative stress-induced cellular apoptosis to a significant extent, in a dose-dependent manner. These authors also found that CNL prevents DNA strand breakage induced by ONOO. Wakamatsu el al.2 proposed that CNL is more efficient as an alkyl peroxyl radical scavenger than R-tocopherol, vitamin C, β-carotene, rutin, and quercetin.2 Taking into account that the reactivity of peroxyl radicals is significantly lower than that of other reactive oxygen species (ROS), canolol seems to be a promising chemical agent to prevent and fight oxidative stress (OS). This is a very desirable property because OS has been associated with the development of a large number of health disorders, such as cancer,5 cardiovascular disorders,6 atherosclerosis,7 and Alzheimer’s disease.8 Surprisingly, there is very scarce information currently available on the free radical scavenging activity of canolol. Accordingly, it is the main aim of this work to study in detail the reaction of CNL with the hydroperoxyl radical and to estimate the rate constant and the contributions of different mechanisms and sites of reaction to the overall •OOH radical scavenging activity of this compound. The tested mechanisms are radical adduct formation (RAF), hydrogen atom transfer (HAT), and single electron transfer (SET). Kinetic data are also provided for the first time, and the influence r 2011 American Chemical Society
of the polarity of the environment on the canolol’s •OOH scavenging activity has been assessed.
’ COMPUTATIONAL DETAILS Geometry optimizations and frequency calculations have been carried out using the M05-2X functional9 and the 6-311þG(d,p) basis set. The M05-2X functional has been recommended for kinetic calculations by their developers,10 and it has been also successfully used to that purpose by independent authors.1119 Geometry optimizations and frequency calculations have been carried out in solution, using the SMD continuum model20 and pentylethanoate and water as solvents to mimic lipidic and aqueous environments. Unrestricted calculations were used for open-shell systems, and local minima and transition states were identified by the number of imaginary frequencies (NIMAG = 0 or 1, respectively). In the case of the transition states, it was verified that the imaginary frequency corresponds to the expected motion along the reaction coordinate, by intrinsic coordinate calculations (IRC). All the electronic calculations were performed with Gaussian 09 package of programs.21 Thermodynamic corrections at 298 K were included in the calculation of relative energies. We have not corrected interaction energies for basis set superposition errors (BSSE) because it has been demonstrated that counterpoise corrections overcorrect the BSSE22 and worsens the results.23,24 Received: March 8, 2011 Revised: May 25, 2011 Published: May 30, 2011 8590
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The solvent cage effects have been included according to the corrections proposed by Okuno,25 taking into account the free volume theory.26 These corrections are in good agreement with those independently obtained by Ardura et al.27 and have been successfully used by other authors.2834 The expression used to correct Gibbs free energy is 0 ð2n 2Þ ΔGFV ðn 1Þg sol = ΔGsol RTfln½n10
ð2Þ
where kB and h are the Boltzmann and Planck constants, ΔG6¼ is the Gibbs free energy of activation, σ represents the reaction path degeneracy, accounting for the number of equivalent reaction paths, and k accounts for tunneling corrections. The tunneling corrections defined as the Boltzmann average of the ratio of the quantum and the classical probabilities were calculated using the zero curvature tunneling corrections (ZCT).38 TST has been recently proven to be enough for properly describing chemical reactions between free radicals and anitoxidants.39 It should be taken into account, however, that this is not necessarily the case for all radicalmolecule reactions, but it should be for systems that are chemically similar to that studied in ref 39, which is certainly the case of the system studied in the present work. The branching ratios of the different reaction channels, which represent the percent of their contribution to the overall reaction, have been calculated as Γi ¼
ki 100 koverall
system
ð1Þ
where n represents the molecularity of the reaction. According to expression 1, the cage effects in solution cause ΔG to decrease by 2.54 kcal/mol for bimolecular reactions, at 298.15 K. The rate constants (k) were calculated using conventional transition state theory (TST)3537 and 1 M standard state as kB T ðΔG6¼Þ=RT e k ¼ σk h
Table 1. T1 Diagnostic for Transition States that Involved H Abstractions, by Oxygenated Radicals, from the OH Moiety in Different Systems
ð3Þ
where i represents each particular channel. The electronic spectra have been computed using the timedependent density functional theory (TD-DFT), based on vertical excitations involving the three lowest-lying excited states.
’ RESULTS AND DISCUSSION Multireference Diagnostics. Before starting the study of the system of interest with M05-2X, which is based on a singledeterminant reference state, it is important to assess whether such a formalism is suitable. In recent publications, Tishchenko et al.40,41 proposed that the transition states corresponding to the H abstraction from the hydroxyl group in phenol by •OOCH3,40 and from the hydroxyl group in vinyl alcohol by •OH,41 are affected by multireference effects. These findings may lead to the conclusion that H transfers from OH groups (linked to π-electron systems) to oxygenated radicals present multireference character. In a more recent publication, by the same group,42 it was found that the transition state of the H abstraction, by •OOH, from the hydroxyl group in methanol, also presents significant multireference character, according to the T1 diagnostic. This suggests that multireference issues may also affect saturated systems. Moreover, because it has been shown that density functionals with a high fraction of HartreeFock (HF) exchange are often inaccurate for multireference systems,43 they would not be properly described using the M05-2X functional.
a
T1 diagnostic
ethanol þ •OH
0.044
phenol þ •OOCH3
0.044
phenol þ •OH
0.041
methanol þ •OOH
0.048a
canolol þ •OOH
0.023
From ref 42.
Therefore, the reliability of this functional has been tested. We have performed the T1 diagnostic at the CCSD(T)/6-311þG(d)//M05-2X/6-311þG(d,p) level of theory for the transition states corresponding to the H abstractions mentioned in the previous parragraph and also for that of canolol þ •OOH, when the abstraction takes place from the OH moiety. In addition, the T1 diagnostic has also been applied to the H abstraction from the hydroxyl group in phenol by •OH. The values obtained from the T1 diagnostic are presented in Table 1. The value for the methanol þ •OOH system was taken from ref 42 and was obtained at the CCSD(T)/aug-cc-pVDZ//M06-2X/MG3S level of theory. It has been established that a T1 value of 0.02 or greater indicates a significant multireference character for closed-shell systems. For open-shell systems, on the other hand, the benchmark value accepted so far is considerably larger and is equal to 0.045.44 The T1 values obtained for the ethanol þ •OH and phenol þ •OOCH3 systems are close to, but slightly lower than, this limit. For the phenol þ •OH system, the T1 value is lower than the limit (0.041), but much higher than that obtained for the canolol þ •OOH system. However, the rate constant calculated using the same level of theory employed in the present work, ZCT/TST and M05-2X/6-311þG(d,p), is only 2.17 times lower than the experimental value.45 This corresponds to an error of only 0.45 kcal/mol 6 , which is significantly below the expected accuracy of even in ΔG¼ high levels of theory. This is also another example of the good performance of the Minnesota’s DFT formalisms. The largest T1 value is the one reported for the methanol þ •OOH, which exceeds the 0.045 limit by 0.003. However, Alecu and Truhlar42 reported that, in this particular case, “The fact that M05 and M06 are outperformed by their 2X counterparts, which contain twice the percentages of Hartree-Fock exchange further indicates that the reactions studied here are not significantly affected by multireference effects, because in the cases characterized by significant multireference character, one would expect increasing the fraction of HF exchange to diminish the quality of the results” (quotation from ref 42). The smallest T1 value, among the tested transition states, corresponds to that of the canolol þ •OOH system (0.023). Therefore, it can be safely stated that it does not present multireference character and, therefore, that the results presented in this work, from M05-2X calculations, are reliable. The T1 value obtained for this system is substantially lower than those obtained for the other tested systems. We have no explanation for this finding other than that not all H abstractions from OH groups are equally susceptible to multireference effects. In any case, it seems that it is not possible to predict a priori if such effects would be present based only on the kind of reaction that takes place. Moreover, on the basis of these and previous results, it can be stated that M05-2X calculations are also reliable for describing this kind of system. 8591
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Figure 1. Canolol and its sites of reaction (blue represents HAT sites and red RAF sites).
Table 2. Gibbs Free Energies of Reaction (ΔG) and Gibbs Free Energies of Activation (ΔG6¼), at 298.15 K, in kcal/mol, with Respect to the Isolated Reactants penthylethanoate ΔG6¼
channel
ΔG
SET HAT
62.73
3a
13.02
23.94
4a
7.03
5a
13.67
3ah
water ΔG 21.55 10.60
22.96
14.49
12.05
11.36
24.79
11.04
23.50
23.40
5ah
ΔG6¼
22.68
24.39
22.39
RAF 1 2
15.85 12.48
21.80 20.40
14.29 10.61
19.57 16.91
3
15.09
23.20
13.08
19.24
4
5.13
17.72
3.82
13.66
5
14.30
20.79
12.22
18.57
6
13.83
20.09
11.88
17.00
7
6.40
19.14
4.31
18.08
8
6.03
14.20
8.59
12.12
Canolol against Oxidative Stress. The structure of CNL and the numbers assigned in this work to each site of reaction are shown in Figure 1. The antioxidant activity of HSA can take place through different mechanisms, as for many other compounds.4651 Those considered in this work are the following. Radical adduct formation (RAF), on sites 18
CNL þ •OOH f ½CNLOOH• Hydrogen atom transfer (HAT), from sites 3a5a CNL þ •OOH f CNLðHÞ• þ H2 O2 Single electron transfer (SET) CNL þ •OOH f CNL•þ þ OOH The relative electronic energies, with respect to the isolated reactants, are reported in Table 1S in the Supporting Information. The Gibbs free energies of reaction (ΔG) and Gibbs free energies of 6 ), at 298.15 K, for the different mechanisms and activation (ΔG¼ reaction sites are provided in Table 2. As these values show, the SET mechanism was found to be endergonic for the reaction of CNL with •OOH, both in polar and in nonpolar media. Therefore, this mechanism has been ruled out for the •OOH scavenging activity of canolol. However, it should be noticed that this finding does not exclude SET as a viable mechanism for the reactions of CNL with other free radicals, in particular, with those with high
Figure 2. Optimized geometries, in penthylthanoate (water) solution, of transition states corresponding to the RAF mechanism.
electro-accepting character. In fact, we tested such a viability for the CNL þ •OH reaction and found that the SET process is exergonic by 1.54 kcal/mol in aqueous solution. Moreover, once the CNL radical cation is formed, the deprotonation process is predicted to occur spontaneously in aqueous solution, from site 4a, (ΔG = 10.75 kcal/mol). For the HAT and RAF mechanisms, only one channel of reaction was found to be exergonic in each case, regardless of the polarity of the environment. They are those involving the H transfer from the OH moiety in CNL (site 4a) and the •OOH addition to site C8. In general, the thermochemical viability of all the studied channels of reaction increases in aqueous solution, compared with the similar processes in lipidic media. The fully optimized geometries of the transition states (TS) corresponding to RAF channels are shown in Figure 2. In general, the TSs were found to be earlier in aqueous solution than in nonpolar media, suggesting that the polarity of the environment favors the reactivity. This is confirmed by the finding that the barriers of reaction are lower in aqueous solution (Table 2). The earliest TS is that associated with the •OOH addition to site C8, with the distance of the forming bond equal to 2.03 and 2.08 Å, in lipid and aqueous solutions, respectively. This channel also has the lowest barrier among the RAF channels. The structures of the TSs arising from the HAT processes are shown in Figure 3. For the H transfer from sites 3a and 5a two different TSs were located. For the kinetic calculations, we have used the single structure approximation. One of them presents a H-bondlike interaction between the H atom in the •OH fragment and the O atom in the hydroxyl moiety of CNL (TS3ah, TS5ah) and the other without such an interaction (TS3a, TS5a). TS4a also presents this kind of stabilizing interaction, in this case, involving the O atom bonded to C3 in canolol. This TS corresponds to the HAT channel with the lowest barrier. Moreover, it has the lowest barrier of all the studied channels, regardless of the mechanism of reaction, indicating the highest reactivity of this site toward •OOH radicals. The geometrical parameters related to H-bond-like interactions are provided in the Supporting Information (Table 2S). Because spin contamination is an issue that can affect the accuracy of energies and structures of open-shell systems, we have checked the spin-squared values for all the open-shell 8592
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Figure 3. Optimized geometries, in penthylthanoate (water) solution, of transition states corresponding to the HAT mechanism.
Table 3. Branching Ratios (Γ) and Rate Constants (k) of the Different Channels of Reaction and Overall Rate Coefficient (L mol1 s1), at 298.15 K penthylethanoate Γ
k 5
water Γ
k 4
site 3a
7.84 10
∼0
3.83 10
site 4a
6.81 105
99.93
2.45 106
Site 5a
2.05 105
∼0
5.13 104
∼0
site 1
1.30 103
∼0
5.59 102
∼0
site 2
2
1.37 10
∼0
4.97 100
∼0
site 3 site 4
1.22 104 1.27 100
∼0 ∼0
9.85 102 1.20 103
∼0 0.05
site 5
7.13 103
∼0
3.02 101
∼0
site 6
2.32 10
2
∼0
4.31 100
∼0
site 7
1.15 101
∼0
6.90 101
∼0
site 8
4.83 102
overall
6.82 105
0.07
1.61 104
∼0 99.30
0.65
2.47 106
species, before and after annihilation of the first spin contaminant; and their percent errors with respect to the expected value. These results are provided in the Supporting Information (Tables 3S6S). In all cases, the deviations from the ideal value (ÆS2æ = 0.75) were lower than 8.7% and 0.4% before and after annihilation of the first spin contaminant. It has been established that, for differences within 10% error, the obtained results can be trusted.52,53 Therefore, the spin contamination can be considered negligible for all the radicals species studied in this work and their energy values are reliable. The rate constants calculated for all channels of reaction, as well as the overall rate coefficient corresponding to the CNL þ •OOH reaction, are reported in Table 3. It has been assumed that neither mixing nor crossover between different pathways occurs, and therefore, the overall rate coefficient (k) has been calculated as the sum of the rate coefficients of each channel. The tunneling corrections and the reaction path degeneracies are provided in the Supporting Information (Table 7S). According to the overall rate coefficients, CNL is predicted to react about 3.6 times faster in aqueous solution than in nonpolar
media. Because the solubility of canolol is expected to be higher in nonpolar than in polar media, this behavior is in line with the previously proposed “polar paradox”.54 The tunneling corrections (k) have been estimated taken into account the prereactant complex, and the k values were found to be 475.4 and 83.5 for the HAT process from site 4a, in lipid and aqueous solutions, respectively. The values of the overall rate coefficients reported in Table 3 indicate that the efficiency of canolol as a OOH radical scavenger is similar to that of carotenes (∼105106 M1 s1),55 higher than that of allicin (∼8 103 M1 s1),56 much higher than that of melatonin (∼2 101 M1 s1),57 and about 10 times lower than that of 2-propenesulfenic acid (∼2.6 107 M1 s1).56 The calculated values of the overall rate coefficients are similar to those estimated, from experiments, for the reactions of alkylperoxy radicals with R-tocopherol, which range from 1.5 105 to 7.9 106 M1 s1.58 This is a logical finding, due to the structural similarities of the compared compounds, and supports the reliability of the presented calculations. This also supports the proposal of Koski et al.1 that the efficiency of canolol for scavenging this kind of radicals is similar to those of tocopherols. It seems worthwhile to call attention on the fact that, due to the relative low reactivity of •OOH, compared with other ROS, overall rate coefficients in the order of 106 M1 s1 indicate that CNL is a very good scavenger. However, it can react much faster with other ROSs. For example, with •OH, considering only SET processes, CNL is predicted to react at diffusion-limited rates (7.8 109 M1 s1). This value was calculated using the Marcus theory,59 which relies on the transition-state formalism and defines the ET activation barrier (ΔG6¼ ET) as !2 λ ΔG0ET 6¼ 1þ ð4Þ ΔGET ¼ 4 λ where (ΔG0ET is the free energy of reaction and λ is a reorganization term. For the SET reaction between CNL and •OH, in aqueous solution, λ = 5.79 kcal/mol and ΔG6¼ ET = 1.69 kcal/mol. The rate constants (k) calculated that way is in the diffusionlimit regime. Accordingly, the apparent rate constant (kapp) cannot be directly obtained from TST calculations. In the present work, the CollinsKimball theory is used for that purpose60 kapp ¼
kD kact kD þ kact
ð5Þ
where kact is the thermal rate constant, obtained from TST calculations (eq 2), and kD is the steady-state Smoluchowski61 rate constant for an irreversible bimolecular diffusion-controlled reaction kD ¼ 4πRDAB NA
ð6Þ
where R denotes the reaction distance (and has been taken as 2.0 and 2.6 Å for RAF and HAT processes, respectively), NA is the Avogadro number, and DAB is the mutual diffusion coefficient of the reactants A (OH radical) and B (canolol). DAB has been calculated from DA and DB according to ref 62; DA and DB have been estimated from the StokesEinstein approach63 D¼
kB T 6πηa
ð7Þ
where kB is the Boltzmann constant; T is the temperature; η denotes the viscosity of the solvent, in our case, water (η = 8.91 104 Pa s) and pentylethanoate (η = 8.62 104 Pa s); and a is the radius of the solute (aOOH = 5.27 Å and aCNL = 8.35 Å). 8593
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of the cellular bilayer interfaces. So far, canolol is considered to be a good antioxidant for preventing the oxidation of canola oil. Our results show that this role can be of great importance also in the human body after ingestion; that is, canolol not only is a preserving agent for oil but could also be used as a dietary supplement to prevent and fight oxidative stress in living organisms. The same strategy used by nature to keep canola seeds DNA safe can be used by us to help protecting our DNA, and other important biomolecules, from oxidation.
Figure 4. Computed UVvis spectra of canolol and the main product of its reaction with •OOH.
It was found that HAT from the phenolic moiety in canolol is the main channel of reaction, contributing to the overall reactivity of CNL toward •OOH by more than 99%, regardless of the polarity of the environment. The •OOH addition to site C8 is a minor channel, and the reactivity of all the other sites is negligible. Accordingly, only one product of reaction is expected to be formed to a significant extent, that arising from channel 4a. The UVvis spectra of canolol and of the main product of reaction have been computed and are reported in Figure 4. Whereas canolol shows only one band of absorption with λmax = 264 nm, the oxidation product yielded from HAT at site 4a shows two absorption bands significantly red shifted with respect to that of canolol. They appear at wavelengths equal to 452 and 592 nm. This means that the evolution of the CNL þ •OOH reaction can be followed using this technique, provided that the experiments are conducted fast enough to capture the intermediate formed in the first step of the oxidation. This information is expected to be useful to further experimental investigations on the title reaction. It seems important to make some remarks on the predicted free radical scavenging activity of canolol. It is highly efficient for scavenging a low-reactive free radical (•OOH), regardless of the polarity of the environment. Canolol is expected to be present in both lipid and aqueous media, because the octanol/water partition coefficient of 2,6-dimethoxyphenol is 1.1,64 and both compounds are structurally similar. Therefore, CNL is expected to have the ability of crossing physiologic barriers and to quickly transport into the cells,65 which is a desirable characteristic for a good antioxidant.6671 According to the results presented in this work, CNL can react with ROS through a variety of mechanisms. The preponderant one would be influenced by the nature of the reacting radical. For example, even though the main mechanism of the CNL þ •OOH reaction is HAT, and the SET mechanism is not viable in this case, CNL is predicted to react with •OH through SET at a diffusion-controlled rate. This is in line with previous reports showing that the course of the reactions with different ROS depend not only on the nature of the scavenger but also on the reactivity and structure of the radical.57,72 Considering all these aspects together, canolol is proposed to be a very good, broad-spectrum antioxidant capable of reacting via RAF, HAT, and SET in both polar and lipid media. Moreover, CNL might be even more efficient than carotenes as a free radical scavenger, because the latter one would only be present in the lipidic phase, whereas CNL is expected to be present at both sides
’ CONCLUSIONS The OOH radical scavenging activity of canolol (CNL) has been studied in aqueous and lipid solutions, and CNL is predicted to react about 3.6 times faster in lipid media than in aqueous solution. The OOH radical scavenger activity of canolol is predicted to be similar to that of carotenes, higher than that of allicin, and much higher than that of melatonin. The overall rate coefficients are predicted to be 2.5 106 and 6.8 105 M1 s1, in aqueous and lipid media, respectively. Branching ratios for the different channels of reaction are reported for the first time. It was found that HAT from the phenolic moiety in canolol is the main channel of reaction, contributing to the overall reactivity of CNL toward •OOH by more than 99%, regardless of the polarity of the environment. ’ ASSOCIATED CONTENT
bS
Supporting Information. Distances, bond angles, and dihedral angles for the TSs with H-bond interactions; spinsquared values for the open-shell species, before and after annihilation of the first spin contaminant; their percent errors with respect to the expected value; tunneling corrections; reaction path degeneracies; and electronic energies, relative to isolated reactants. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*E-mail:
[email protected].
’ ACKNOWLEDGMENT We gratefully acknowledge the Laboratorio de Visualizacion y Computo Paralelo at Universidad Autonoma MetropolitanaIztapalapa and the Direccion General de Servicios de Computo Academico (DGSCA) at Universidad Nacional Autonoma de Mexico. This work is a result of the FONCICYT 545 Mexico-EU ‘‘RMAYS’’ network, Project No. 94666. ’ REFERENCES (1) Koski, A.; Pekkarinen, S.; Hopia, A.; Wahala, K.; Heinonen, M. Eur. Food Res. Technol. 2003, 217, 110. (2) Wakamatsu, D.; Morimura, S.; Sawa, T.; Kida, K.; Nakai, C.; Maeda, H. Biosci., Biotechnol., Biochem. 2005, 69, 1568. (3) See, for example: (a) Burton, G. W.; Ingold, K. U. Acc. Chem. Res. 1986, 19, 194. (b) de Heer, M. I.; Mulder, P.; Korth, H. G.; Ingold, K. U.; Lusztyk, J. J. Am. Chem. Soc. 2000, 122, 2355. (c) Litwinienko, G.; Ingold, K. U. Acc. Chem. Res. 2007, 40, 222. (4) Kuwahara, H.; Kanazawa, A.; Wakamatu, D.; Morimura, S.; Kida, K.; Akaike, T.; Maed, H. J. Agric. Food Chem. 2004, 52, 4380. 8594
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