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J. Phys. Soc. Jpn. 87, 084802 (2018) [5 Pages]
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Cyclic Bond Formation of Rhododendrol-quinone and Dopamine-quinone: Effects of Proton Rearrangement

Ryo Kishida1,, and Hideaki Kasai2,3
+ Affiliations
1Department of Biomaterials, Faculty of Dental Science, Kyushu University, Fukuoka 565-0871, Japan2National Institute of Technology, Akashi College, Hyogo 674-8501, Japan3Graduate School of Engineering, Osaka University, Suita, Osaka 565-0871, Japan
Received March 12, 2018; Accepted May 22, 2018; Published July 12, 2018

The synthesis of melanin pigment involves intramolecular cyclic bond formation between benzene ring and side chain moieties of o-quinone as a necessary process for o-quinone conversion into a cyclic catechol, i.e., cyclization. Dopamine (DA)-quinone and rhododendrol (RD)-quinone undergo cyclic C–N and C–O bond formation, respectively. A previous theoretical study revealed that RD-quinone requires hydroxy deprotonation or quinonic protonation for cyclic C–O bond formation. In this study, the theoretical model was extended to an (H2O)n-quinone interacting system (\(n = 3,4\)) so that protonation and deprotonation governed by H2O molecules are incorporated. Density functional theory (DFT)-based simulation showed that RD-quinone can undergo proton-rearrangement-assisted cyclic C–O bond formation with a moderate barrier height which is still higher than that for DA-quinone cyclic bond formation. The DFT-based simulation also showed that both DA-quinone and RD-quinone can undergo proton-rearrangement-assisted C–O bond formation for the addition of water with slightly higher activation energies than those of cyclic bond formation. The obtained mechanism is markedly different from that for DA-quinone, which can sequentially undergo the cyclic C–N bond formation and proton rearrangement.

©2018 The Physical Society of Japan
https://doi.org/10.7566/JPSJ.87.084802
1. Introduction

The oxidation of tyrosine/dopa or similar p-substituted phenols/catechols results in the formation of o-quinones. Animals utilize the oxidation of tyrosine to dopaquinone (a kind of o-quinone) in their skin and hair to synthesize a pigment called melanin. As serious diseases related to the melanin-synthesizing cells (melanocytes), melanoma (a skin cancer arising from melanocytes), and vitiligo (a patchy depigmentation with the loss of melanocytes) have extensively been investigated.1,2) In parallel with investigations on these diseases, a certain kind of o-quinone has been reported to cause melanocyte-specific cytotoxicity.3) Such cytotoxicity can play both positive and negative roles in melanocyte pathophysiology; it can be exploited for anti-melanoma therapy and depigmentation of remaining pigmented patches in vitiligo, but can also increase the risk of leukoderma as an adverse effect of the use of cosmetics. Artificially synthesized melanin-like pigments derived from o-quinones have also attracted broad attention due to their specific properties (e.g., conductance switching and photoconductivity)4,5) and several possible applications (e.g., plating and tissue engineering).6,7) Thus, the understanding of o-quinone chemistry is of great importance for the fields of medical application and materials engineering.

The formed o-quinones are reactive towards nucleophiles (electron pair donors).8,9) For instance, cellular thiols such as cysteine and glutathione (GSH) can immediately bind o-quinones through the sulfhydryl group (–SH) (Fig. 1). The binding of thiols can induce cytotoxic effects in various ways. Considering that GSH acts as an antioxidant, the concentration of reactive oxygen species (ROS) can be increased by the depletion of GSH.10) The binding of protein thiols by o-quinones may trigger a distinct immune response due to structural changes of proteins.11,12) The binding of cysteine to an o-quinone results in the formation of a yellow to reddish brown sulfur-containing pigment (pheomelanin), which can photosensitize oxygen into ROS.13,14) If the p-substituent is a hydrocarbon chain terminated by a nucleophilic group (e.g., –NH2 or –OH), intramolecular cyclization (ring closure reaction) can also take place as a competitive reaction (Fig. 1), and then a dark pigment (eumelanin) is generated via several subsequent spontaneous reactions. Melanin synthesis involves some reaction branchings due to competitive reactions.15–17) As briefly mentioned already, the competition involving o-quinones (i.e., cysteine binding and cyclization) determines the eumelanin/pheomelanin synthetic branching. Completion of the cyclization effectively deactivates the o-quinone itself towards a competing cytotoxic reaction, thiol binding.17) Thus, the competition involving o-quinones is important for understanding cytotoxicity in melanocytes.


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Figure 1. Oxidation to form o-quinone [(a) DA-quinone and (b) RD-quinone] and subsequent competing reactions (cyclization, cysteine binding, and addition of water). Note that the catechols resulting from the competing reactions are easily oxidized to form their quinones. Furthermore, RD-cyclic-quinone and RD-hydroxy-quinone can interconvert to each other via the addition or elimination of water.

In recent years, rhododendrol (RD), a plant-derived phenolic compound, has also been reported to cause toxicity specifically for melanocytes.18) RD had been used as a skin-whitening agent in Japan until 2013, when it was recalled because of a cytotoxic adverse effect causing leukoderma. The mechanistic understanding of RD cytotoxicity along with the relevant chemistry is of great importance to develop cosmetics without cytotoxic concerns. Several (bio-) chemical experiments have shown the production of melanin-like pigment in RD metabolisms and its pro-oxidant activity.19,20) Furthermore, the enzymatic oxidation of RD has been confirmed along with the resulting o-quinone (RD-quinone).21,22) As compared with the case of dopaquinone, the cyclization of RD-quinone was found to proceed with a slower rate.21,23) In addition to cyclization and thiol binding, as another possible competing reaction, the addition of water to RD-quinone was also indicated [Fig. 1(b)].21) Considering the cytotoxic effects of thiol binding, RD-quinone cytotoxicity is partly due to its slow cyclization. Nevertheless, it must also be noted that, for some reductant molecules, eumelanin-like pigment resulting from RD-quinone cyclization shows higher pro-oxidant activity than pheomelanin-like pigment resulting from the binding of cysteine to RD-quinone.20)

o-Quinone cyclization proceeds via several elementary processes including bond formation between a benzene ring carbon and a nucleophile atom (e.g., N or O). The reactivity towards this cyclic bond formation is essentially dependent on the p-substituent electronic properties.24) Our recent studies have revealed that the cyclization proceeds via electronic charge redistribution from a nucleophile to a quinonic carbonyl group.24) This indicates that the cyclic bond formation is facilitated by the presence of positive charges (e.g., protons) near the quinonic carbonyl oxygen. We previously showed that RD-quinone hardly undergoes cyclic C–O bond formation without hydroxy deprotonation or quinonic protonation.25) Since quinonic oxygens and alcoholic hydroxy groups are a weak base and weak acid, respectively, such (de)protonation is not energetically favorable. Based on this finding, a slightly modified mechanism was proposed with the emphasis on the addition of water rather than the cyclization.26) However, a direct comparison between the two reactions has not yet been conducted. In contrast, cyclic C–N bond formation as in dopamine (DA)-quinone (a precursor of melanin in the brain) [Fig. 1(a)] can proceed without amino deprotonation or quinonic protonation.24) It should also be noted that the cyclization of RD-quinone was reported as a base-catalyzed reaction,21) indicating the importance of deprotonation processes. These findings motivated us to further study the mechanism(s) of RD-quinone cyclization in comparison with that of DA-quinone by identifying a possible cyclic bond formation pathway.

As demonstrated in previous studies, coupling between cyclic bond formation and protonation/deprotonation processes is inevitable for some o-quinones. Towards the general modeling of cyclization, investigation of the effect of such protonation/deprotonation must be conducted. Here, we only discuss cyclic bond formation and proton rearrangement from a nucleophile atom (e.g., N or O) to a quinonic oxygen (O4). Note that the completion of cyclization (and the addition of water) also requires subsequent proton rearrangement from the attacked carbon (C6) to a remaining quinonic oxygen (O3). For simplicity, we do not discuss the details of the subsequent proton rearrangement. In this study, we extended the theoretical model to an (H2O)n-quinone interacting system (\(n=3,4\)) so that protonation and deprotonation governed by H2O molecules are incorporated. Using this interacting model (\(n=3\)), we conducted a density functional theory (DFT)-based simulation to investigate the mechanisms of the initial step of cyclization for two o-quinones, viz. DA-quinone and RD-quinone. We also investigated the energy profile for the initial step of the addition of water using the interacting model (\(n=4\)). The use of this interacting model enables us to systematically compare the cyclization and the addition of water. From our results, for RD-quinone, cyclic C–O bond formation and proton rearrangement were shown to be coupled with each other. This mechanism is markedly different from that for DA-quinone, which can sequentially undergo cyclic C–N bond formation and proton rearrangement.

2. Methods

First-principles calculations based on DFT27,28) were performed with Becke's three-parameter hybrid functional29) combined with the Lee–Yang–Parr correlation functionals (B3LYP).30) Calculations were carried out with the 6-31++G(d,p) basis set using the Gaussian 09 computational package.31) Note that the use of B3LYP/6-31++G(d,p) for melanin synthetic intermediates (including DA-quinone) has been validated in our previous studies.15,24)

To model the stabilization by the dielectric response of surrounding water molecules, the integral equation formalism polarizable continuum model (IEF-PCM)32) was used for both the single point calculations and the structural optimizations.

6-Carbon (C6) [Figs. 1(a) and 1(b)] was chosen as the site for –NH2 or –OH attack based on previous studies.33,34) Correspondingly, the C6–N or C6–O distance was considered to be involved in the reaction coordinate. Proton rearrangement requires dissociation of the amino N–H bond of DA-quinone or the hydroxy O–H bond of RD-quinone. Thus, the N–H or O–H distance was also considered as the variables involved in the reaction coordinate. All degrees of freedom except for the two variables involved in the reaction coordinate were allowed to relax during the calculation.

3. Results and Discussion

We constructed (H2O)3-bound DA- and RD-quinone models and defined two variables (\(R_{\text{C6--N}}/R_{\text{C6--O}}\) and \(R_{\text{N--H}}/R_{\text{O--H}}\)) as shown in Fig. 2. First, we calculated the one-dimensionally projected potential energy curve as a function of \(R_{\text{C6--N}}\) or \(R_{\text{C6--O}}\) with a frozen \(R_{\text{N--H}}\) or \(R_{\text{O--H}}\) (Fig. 3). DA-quinone shows an energy maximum (0.31 eV) at 2.08 Å, whereas RD-quinone shows a monotonically increasing potential energy with decreasing \(R_{\text{C6--O}}\). The obtained barrier height (and the bond formation energy) for DA-quinone cyclic bond formation is lower than the previously reported value.24) This difference is considered to be due to the strengthened hydrogen bond between H2O and a quinonic carbonyl oxygen (O4) by cyclic bond formation. The cyclic bond formation proceeds via electronic charge redistribution from –NH2 to O4.24) Thus, the enhanced negative charge at O4 must strengthen the hydrogen bond with H2O.


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Figure 2. (Color online) (Left) (H2O)3-bound DA-quinone model and (right) (H2O)3-bound RD-quinone model. Two degrees of freedom (\(R_{\text{C6--N}}/R_{\text{C6--O}}\) and \(R_{\text{N--H}}/R_{\text{O--H}}\)) involved in the reaction coordinate are defined.


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Figure 3. (Color online) One-dimensionally projected potential energy curves as a function of \(R_{\text{C6--N}}\) or \(R_{\text{C6--O}}\) with the frozen \(R_{\text{N--H}}\) or \(R_{\text{O--H}}\). The origin of the energy was defined by the total energy of the C6–N or C6–O dissociated (optimized) structure.

Next, we calculated the two-dimensionally projected potential energy surface as a function of \(R_{\text{C6--N}}\) and \(R_{\text{N--H}}\) or \(R_{\text{C6--O}}\) and \(R_{\text{O--H}}\) (Figs. 4 and 5, respectively). As shown in Fig. 4, the reaction of DA-quinone proceeds via three energy minima, indicating the presence of an intermediate (cyclic-bonded) state. This confirms that DA-quinone can sequentially undergo cyclic C–N bond formation and proton rearrangement. In contrast, Fig. 5 shows only two energy minima, indicating the absence of an intermediate (cyclic-bonded) state. Figure 5 clearly shows that, with the aid of H2O molecules, RD-quinone can undergo proton-rearrangement-assisted cyclic C–O bond formation with a moderate barrier height (0.81 eV) which is still higher than that for DA-quinone cyclic bond formation (0.31 eV). The obtained results show that the requirement of hydroxy deprotonation or quinonic protonation is not a proof of completely inactive cyclization, as considered in a previous report.26) Note that the potential energy surfaces include regions showing a nonsmooth potential decrease. This suddenly changing potential energy is due to proton rearrangement; an eliminated proton is transferred to O4 through the hydrogen-bonding network of (H2O)3.


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Figure 4. (Color online) Contour plot of potential energy surface as a function of \(R_{\text{C6--N}}\) and \(R_{\text{N--H}}\) (defined in Fig. 2) for DA-quinone. The contour spacing is 0.05 eV. Cyclic bond formation roughly proceeds from the pink star to the purple star. The origin of the energy was defined by the total energy of the C6–N dissociated (optimized) structure.


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Figure 5. (Color online) Contour plot of potential energy surface as a function of \(R_{\text{C6--O}}\) and \(R_{\text{O--H}}\) (defined in Fig. 2) of RD-quinone. The contour spacing is 0.05 eV. Cyclic bond formation roughly proceeds from the pink star to the purple star. The origin of the energy was defined by the total energy of the C6–O dissociated (optimized) structure.

For comparison, we also investigated the initial step in the addition of water to DA-quinone and RD-quinone. To estimate the activation barriers, we constructed (H2O)4-bound DA- and RD-quinone models (Fig. 6). As shown in Fig. 7, the barriers are higher than those for the (proton-rearrangement-assisted) cyclic bond formation. Thus, we conclude that the addition of water can proceed with a finite activation energy although the reaction is slower than the cyclization. Note that the potential energy curves include some points showing a nonsmooth potential decrease. In the case of DA-quinone, the nonsmooth potential change is due to proton transfer from H2O (near C6) to amino nitrogen, whereas RD-quinone experiences a sudden change of the hydrogen-bonded quinonic oxygen (from O3 to O4) as well as similar proton transfer to hydroxy oxygen.


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Figure 6. (Color online) (Left) (H2O)4-bound DA-quinone model and (right) (H2O)4-bound RD-quinone model. One degree of freedom (\(R_{\text{H2O--C6}}\)) involved in the reaction coordinate is defined.


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Figure 7. (Color online) One-dimensionally projected potential energy curves as a function of \(R_{\text{H2O--C6}}\). The origin of energy was defined by the total energy of the C6–N or C6–O dissociated (optimized) structure.

In the case of DA-quinone, at neutral pH, the amino nitrogen mainly exists as ammonium ion (–NH3+) (e.g., p\(K_{\text{a}}\) of ethylammonium CH3CH2NH3+ is ca. 1135)), meaning that C–N cyclic bond formation cannot directly take place. Thus, DA-quinone cyclization should be initiated by ammonium deprotonation. A previous kinetic study found that ammonium deprotonation and amino reprotonation can be in quasi-equilibrium because the reprotonation is much faster than the amino attack.33,36,37) This quasi-equilibrium results in the overall constant rate which is proportional to the ammonium acidity constant and to the rate constant for amino substitution. In this paper, we do not explicitly consider the ammonium deprotonation because it is directly amenable to an experimental measurement. In contrast, alcoholic hydroxy groups prefer electroneutral states (e.g., p\(K_{\text{a}}\) of ethanol CH3CH2OH is ca. 1638)).

In this study, the (H2O)n-bound quinone model (\(n=3,4\)) was designed to construct a hydrogen-bonding network from the nucleophile atom to a quinonic oxygen. The predominant factor responsible for determining the activation barrier is considered to be the stabilization of the formed hydronium (or oxonium) ion by surrounding H2O molecules. In contrast, proton transfer itself between two H2O (+ H+) is almost barrierless if the orientation of the two H2O (+ H+) is optimized. Even if the rotation of H2O is considered, the proton transfer barrier can be estimated to be around 0.1 eV.39) As shown in Figs. 2 and 6, the (H2O)n-bound quinone models contain two H2O that stabilize the formed hydronium (or oxonium) ion. Therefore, we expect that our (H2O)3- and (H2O)4-bound models are enough to resolve the reactivity towards the cyclization and the addition of water, respectively.

The obtained results indicate that the cyclic C–O bond formation is less preferable than the cyclic C–N bond formation. As mentioned above, the cyclic bond formation proceeds via electronic charge redistribution from the nucleophile atom to O4.24) As manifested in the ionicity of the C–O bond, which is much higher than that of the C–N bond, electronic charge redistribution from the hydroxy group is considered to be less preferable.

On the basis of our simulated results and the discussion above, o-quinone cyclization mechanisms can be generalized. Weak cyclic bonds (e.g., less covalent C–O bonds) can be formed with the aid of surrounding H2O molecules via proton rearrangement.

4. Conclusions

With the aid of DFT-based calculation, we investigated the mechanisms of the initial step of cyclization for two o-quinones, viz. DA-quinone and RD-quinone, as representative cases. To incorporate protonation and deprotonation governed by H2O molecules, we proposed an (H2O)n-quinone interacting system (\(n=3,4\)).

As a result, we found that, with the aid of H2O molecules, RD-quinone can undergo proton-rearrangement-assisted cyclic C–O bond formation with a moderate barrier height, which is still higher than that for DA-quinone cyclic bond formation. In the case of DA-quinone, cyclic C6–N bond formation can proceed without proton rearrangement.

Thus, for RD-quinone, cyclic C–O bond formation and proton rearrangement are coupled with each other. This mechanism is markedly different from that for DA-quinone, which can sequentially undergo cyclic C–N bond formation and proton rearrangement. This finding provides a mechanistic understanding of o-quinone chemistry and also serves as a foundation for the development of cosmetic science.

From our simulation, further diversity in o-quinone chemistry and its broader application are expected. We believe that the obtained results along with the proposed model shed light on the mechanism of o-quinone cyclization in the generalized sense.

Acknowledgements

This work was supported in part by MEXT Grants-in-Aid for Scientific Research (15H05736, 24246013, 15KT0062, 26248006), a Grant-in-Aid for JSPS Research Fellows (17J01276), the JST ACCEL Program (JPMJAC1501) “Creation of the Functional Materials on the Basis of the Inter-Element-Fusion Strategy and their Innovative Applications”, and the NEDO Project “R&D Towards Realizing an Innovative Energy Saving Hydrogen Society based on Quantum Dynamics Applications”. Some of the numerical calculations presented here were done using the computer facilities at CMC (Osaka University), ISSP, KEK, NIFS, and YITP.

References

  • 1 M. Herlyn, Cancer Metastasis Rev. 9, 101 (1990). 10.1007/BF00046337 Crossref, Google Scholar
  • 2 E. H. Kemp, E. A. Waterman, and A. P. Weetman, Expert Rev. Mol. Med. 3, 1 (2001). 10.1017/S1462399401003362 Crossref, Google Scholar
  • 3 A. D. Katsambas and A. J. Stratigos, Clin. Dermatol. 19, 483 (2001). 10.1016/S0738-081X(01)00182-1 Crossref, Google Scholar
  • 4 J. E. McGinness, Science 177, 896 (1972). 10.1126/science.177.4052.896 Crossref, Google Scholar
  • 5 S. Subianto, G. Will, and P. Meredith, Polymer 46, 11505 (2005). 10.1016/j.polymer.2005.10.068 Crossref, Google Scholar
  • 6 R. A. Sturm, Human Mol. Gene. 18, R9 (2009). 10.1093/hmg/ddp003 Crossref, Google Scholar
  • 7 C. J. Bettinger, J. P. Bruggeman, A. Misra, J. T. Borenstein, and R. Langer, Biomaterials 30, 3050 (2009). 10.1016/j.biomaterials.2009.02.018 Crossref, Google Scholar
  • 8 S. Ito, Pigm. Cell Res. 16, 230 (2003). 10.1034/j.1600-0749.2003.00037.x Crossref, Google Scholar
  • 9 S. Ito and K. Wakamatsu, Photochem. Photobiol. 84, 582 (2008). 10.1111/j.1751-1097.2007.00238.x Crossref, Google Scholar
  • 10 C. D. Villarama and H. I. Maibach, Int. J. Cosmet. Sci. 27, 147 (2005). 10.1111/j.1467-2494.2005.00235.x Crossref, Google Scholar
  • 11 W. Westerhof and M. D’Ischia, Pigm. Cell Res. 20, 345 (2007). 10.1111/j.1600-0749.2007.00399.x Crossref, Google Scholar
  • 12 W. Westerhof, P. Manini, A. Napolitano, and M. d’Ischia, Exp. Dermatol. 20, 92 (2011). 10.1111/j.1600-0625.2010.01200.x Crossref, Google Scholar
  • 13 M. R. Chedekel, S. K. Smith, P. W. Post, A. Pokora, and D. L. Vessell, Proc. Natl. Acad. Sci. U.S.A. 75, 5395 (1978). 10.1073/pnas.75.11.5395 Crossref, Google Scholar
  • 14 A. Napolitano, L. Panzella, G. Monfrecola, and M. d’Ischia, Pigm. Cell Melanoma Res. 27, 721 (2014). 10.1111/pcmr.12262 Crossref, Google Scholar
  • 15 R. Kishida, Y. Ushijima, A. G. Saputro, and H. Kasai, Pigm. Cell Melanoma Res. 27, 734 (2014). 10.1111/pcmr.12256 Crossref, Google Scholar
  • 16 R. Kishida, A. G. Saputro, and H. Kasai, Biochim. Biophys. Acta 1850, 281 (2015). 10.1016/j.bbagen.2014.10.024 Crossref, Google Scholar
  • 17 R. Kishida, H. Kasai, S. M. Aspera, R. L. Arevalo, and H. Nakanishi, J. Electron. Mater. 46, 3784 (2017). 10.1007/s11664-017-5299-x Crossref, Google Scholar
  • 18 M. Sasaki, M. Kondo, K. Sato, M. Umeda, K. Kawabata, K. Y. Takahashi, T. Suzuki, K. Matsunaga, and S. Inoue, Pigm. Cell Melanoma Res. 27, 754 (2014). 10.1111/pcmr.12269 Crossref, Google Scholar
  • 19 S. Ito, M. Okura, Y. Nakanishi, M. Ojika, K. Wakamatsu, and T. Yamashita, Pigm. Cell Melanoma Res. 28, 295 (2015). 10.1111/pcmr.12363 Crossref, Google Scholar
  • 20 S. Ito, M. Okura, K. Wakamatsu, and T. Yamashita, Pigm. Cell Melanoma Res. 30, 63 (2017). 10.1111/pcmr.12556 Crossref, Google Scholar
  • 21 S. Ito, M. Ojika, T. Yamashita, and K. Wakamatsu, Pigm. Cell Melanoma Res. 27, 744 (2014). 10.1111/pcmr.12275 Crossref, Google Scholar
  • 22 S. Ito, W. Gerwat, L. Kolbe, T. Yamashita, M. Ojika, and K. Wakamatsu, Pigm. Cell Melanoma Res. 27, 1149 (2014). 10.1111/pcmr.12300 Crossref, Google Scholar
  •   (23) The cyclization of RD-quinone takes more than 1 min at a weakly acidic pH.21) In contrast, the cyclization of dopa-quinone is too fast to follow by spectrophotometry.8,9,32) Google Scholar
  • 24 R. Kishida, A. G. Saputro, R. L. Arevalo, and H. Kasai, Int. J. Quantum Chem. 117, e25445 (2017). 10.1002/qua.25445 Crossref, Google Scholar
  • 25 R. Kishida, H. Kasai, S. M. Aspera, R. L. Arevalo, and H. Nakanishi, J. Phys. Soc. Jpn. 86, 024804 (2017). 10.7566/JPSJ.86.024804 Link, Google Scholar
  • 26 S. Ito and K. Wakamatsu, Int. J. Mol. Sci. 19, 552 (2018). 10.3390/ijms19020552 Crossref, Google Scholar
  • 27 P. Hohenberg and W. Kohn, Phys. Rev. 136, B864 (1964). 10.1103/PhysRev.136.B864 Crossref, Google Scholar
  • 28 W. Kohn and L. J. Sham, Phys. Rev. 140, A1133 (1965). 10.1103/PhysRev.140.A1133 Crossref, Google Scholar
  • 29 A. D. Becke, J. Chem. Phys. 98, 5648 (1993). 10.1063/1.464913 Crossref, Google Scholar
  • 30 C. Lee, W. Yang, and R. G. Parr, Phys. Rev. B 37, 785 (1988). 10.1103/PhysRevB.37.785 Crossref, Google Scholar
  • 31 M. J. Frisch, G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, G. Scalmani, V. Barone, G. A. Petersson, H. Nakatsuji, X. Li, M. Caricato, A. Marenich, J. Bloino, B. G. Janesko, R. Gomperts, B. Mennucci, H. P. Hratchian, J. V. Ortiz, A. F. Izmaylov, J. L. Sonnenberg, D. Williams-Young, F. Ding, F. Lipparini, F. Egidi, J. Goings, B. Peng, A. Petrone, T. Henderson, D. Ranasinghe, V. G. Zakrzewski, J. Gao, N. Rega, G. Zheng, W. Liang, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, T. Vreven, K. Throssell, J. A. Montgomery, Jr., J. E. Peralta, F. Ogliaro, M. Bearpark, J. J. Heyd, E. Brothers, K. N. Kudin, V. N. Staroverov, T. Keith, R. Kobayashi, J. Normand, K. Raghavachari, A. Rendell, J. C. Burant, S. S. Iyengar, J. Tomasi, M. Cossi, J. M. Millam, M. Klene, C. Adamo, R. Cammi, J. W. Ochterski, R. L. Martin, K. Morokuma, O. Farkas, J. B. Foresman, and D. J. Fox, Gaussian 09 (Revision C.01) (Gaussian, Inc., Wallingford, CT, 2016). Google Scholar
  • 32 J. Tomasi, B. Mennucci, and R. Cammi, Chem. Rev. 105, 2999 (2005). 10.1021/cr9904009 Crossref, Google Scholar
  • 33 E. J. Land, C. A. Ramsden, and P. A. Riley, Arkivoc 2007, 23 (2006). 10.3998/ark.5550190.0008.b02 Crossref, Google Scholar
  • 34 E. J. Land, C. A. Ramsden, and P. A. Riley, Tetrahedron 62, 4884 (2006). 10.1016/j.tet.2006.03.016 Crossref, Google Scholar
  • 35 H. K. Hall, Jr., J. Am. Chem. Soc. 79, 5441 (1957). 10.1021/ja01577a030 Crossref, Google Scholar
  • 36 T. E. Young, J. R. Griswold, and M. H. Hulbert, J. Org. Chem. 39, 1980 (1974). 10.1021/jo00927a057 Crossref, Google Scholar
  • 37 F. Garcia-Carmona, F. Garcia-Canovas, J. L. Iborra, and J. A. Lozano, Biochim. Biophys. Acta 717, 124 (1982). 10.1016/0304-4165(82)90389-0 Crossref, Google Scholar
  • 38 P. Ballinger and F. A. Long, J. Am. Chem. Soc. 82, 795 (1960). 10.1021/ja01489a008 Crossref, Google Scholar
  • 39 N. Agmon, Chem. Phys. Lett. 244, 456 (1995). 10.1016/0009-2614(95)00905-J Crossref, Google Scholar

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