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A TD-DFT study on triplet excited-state properties of curcumin and its implications in elucidating the photosensitizing mechanisms of the pigment
Chemical Physics Letters 409 (2005) 300–303 www.elsevier.com/locate/cplett
A TD-DFT study on triplet excited-state properties of curcumin and its implications in elucidating the photosensitizing mechanisms of the pigment Liang Shen, Hong-Fang Ji, Hong-Yu Zhang
*
Shandong Provincial Research Center for Bioinformatic Engineering and Technique, Center for Advanced Study, Shandong University of Technology, Zhangzhou Road 12 #, Zibo 255049, PR China Received 21 March 2005; in final form 27 April 2005 Available online 8 June 2005
Abstract In this Letter, we present time-dependent density functional theory (TD-DFT)-derived triplet state properties of curcumin in vacuum, benzene and DMSO. Accordingly, the photosensitizing mechanisms of curcumin are explained. It is revealed that in benzene and DMSO, excited curcumin can react with O2 to generate 1O2 and O2 through energy transfer and electron transfer, however, the O2 -generating pathways are different in both solvents. This indicates the potential of TD-DFT in determining the excited-state properties of pigments, which is of significance in getting a deeper insight into the photodynamic mechanisms of photosensitizers. Ó 2005 Elsevier B.V. All rights reserved.
1. Introduction Curcumin [1,7-bis(4-hydroxy-3-methoxyphenyl)-1,6heptadiene-3,5-dione] is a yellow–orange pigment derived from the rhzone of Curcuma longa (Fig. 1A,B) [1,2], which has attracted considerable attention owing to its various significant biological activities, such as radical-scavenging activity, anticarcinogenic activity, antiinflammatory activity and phototoxicity [3–9]. Significant phototoxicity of curcumin against a variety of bacteria and viruses has made curcumin a potential photodynamic drug [10–12]. As the photosensitization of curcumin requires the presence of oxygen [10,12], reactive oxygen species (ROS) is very likely responsible for its phototoxicity. Although some experimental effort has been devoted to elucidating the photosensitive mechanisms of curcumin [11,13], no theoretical study has been performed on this topic, in sharp con*
Corresponding author. Fax: +86 533 278 0271. E-mail address: [email protected] (H.-Y. Zhang).
0009-2614/$ - see front matter Ó 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.cplett.2005.05.023
trast with the radical-scavenging mechanisms of curcumin, which have been intensively investigated by theoretical methods [14–16]. We think this partially results from the difficulty in the theoretical treatment of the short-lived excited-states of curcumin. Considering the successful use of time-dependent density functional theory (TD-DFT) in investigating the molecular excited-state properties [16–19], we attempt to explore the triplet excited-state properties of curcumin by means of TD-DFT, by which we will explain the photosensitive mechanisms of curcumin.
2. Methods Initial structures of curcumin-related compounds were optimized by semiempirical method AM1 [20]. Using these structures as starting points, the geometries were fully optimized by the hybrid B3LYP functional with 6-31G(d,p) Gaussian basis set. Finally, the triplet state properties were calculated by TD-DFT formalism
L. Shen et al. / Chemical Physics Letters 409 (2005) 300–303
301 H
CH3 O
O
O C H2
H
CH3 O
O
O H
O
O
CH3
CH3
O
O
C
H
H
H
O
O
curcumin (A)
curcumin (B) Fig. 1. Molecular structure of curcumin.
with the same basis set [21]. This method has been justified by the calculation of absorption spectrum of curcumin that the method precisely predicts the absorption peak of the pigment [16]. In addition, as the diffusion functions are essential for the treatment of anion and cation radicals, the electron affinities and ionization potentials of curcumin were calculated by a combined method B3LYP/6-31G+(d,p)//B3LYP/6-31G(d,p) [22], which means that B3LYP/6-31G+(d,p) was employed to do a single-point calculation on the basis of B3LYP/ 6-31G(d,p)-optimized structures. During the calculation, both in vacuo and in solvent models were considered. The solvent (benzene and DMSO) effects were involved by employing the self-consistent reaction field (SCRF) method with polarized continuum model (PCM) [23–25]. For molecular oxygen-related parameters, B3LYP/631G+(d,p) was employed to do full-geometry-optimization calculation. All of the calculations were performed with GAUSSIAN 03 package of programs [26].
3. Results and discussion Although curcumin exists in two conformations, A and B (Fig. 1), B predominates in various solvents [13,27], which has also been proved by our theoretical studies [14,16]. Hence, curcumin B is used as starting point of calculation. As it is the triplet state that is responsible for the photosensitizing activity, we focused our study on triplet excited-state of curcumin. 3.1. T1 transition energy Since the lowest T1 transition energy ðDET1 Þ of a photosensitizer is crucial to understanding the photosensitizing mechanisms, we calculated the DET1 of curcumin at first. The DET1 of curcumin in vacuum, benzene and DMSO, 1.95, 1.91 and 1.90 eV (Table 1), are similar
Table 1 The lowest T1 transition energy of curcumin (in eV) DET1
Vacuum
Benzene
DMSO
1.95
1.91
1.90
to one another, indicating that DET1 is slightly influenced by environment. In addition, it is interesting to note that the theoretical DET1 in benzene is close to the experimental value (1.98 eV) [13]. As it is still a challenge to determine DET1 by experiments, the theoretical method seems a proper alternative approach to estimate DET1 of photosensitizers. The DET1 of curcumin is higher than the excited-state energy of singlet oxygen (1O2), 1.06 eV [22], suggesting that curcumin can, in principle, generate 1O2 through energy transfer (Eq. (1)), which agrees well with the experimental finding that curcumin gives birth to 1O2 in benzene with a yield of 0.12 [13]. CurðT1 Þ þ 3 O2 ! CurðS0 Þ þ 1 O2
ð1Þ
3.2. Vertical ionization potential and vertical electron affinity of T1 state Besides energy transfer, photosensitizer also can donate an electron to oxygen and generate superoxide anion radical ðO2 Þ (Eq. (2)). The prerequisite of the reaction is that the summation of vertical ionization potential (VIP) for T1 state (VIPT1) of the pigment and the adiabatic electron affinity (AEA) of molecular oxygen (3O2) is negative. ð2Þ CurðT Þ þ 3 O ! Curþ þ O 1
2
2
In vacuum, the AEA of 3O2 was calculated to be 0.59 eV, which can be compared with the experimental value, 0.45 eV [28]. Whereas, the in vacuo VIPT1 of curcumin was estimated to be 4.81 eV (Table 2), implying that curcumin on T1 state could not donate an electron to oxygen in this case. While in DMSO, the AEA of 3 O2 was calculated to be 3.65 eV and the VIPT1 of curcumin became 3.62 eV (Table 2). Therefore, the O2 can be generated in DMSO by photosensitization of curcumin, which is consistent with the experimental observation [11]. Once O2 is given, other ROS, such as H2O2 and OH can be produced through Fenton reaction [29] or Haber–Weiss reaction [30], which will efficiently amplify the photosensitizing activity of curcumin. In benzene, the AEA of O2 was calculated as 2.33 eV and the VIPT1 of curcumin was 3.87 eV (Table 2), suggesting that O2 could not be generated through this pathway. However, O2 is indeed observed during
302
L. Shen et al. / Chemical Physics Letters 409 (2005) 300–303
Table 2 The vertical ionization potentials (VIPs, in eV) and vertical electron affinities (VEAs, in eV) of curcumin in S0 and T1 states Vacuum Benzene DMSO a b c d e f g
TEpa (in hartree)
TEcb (in hartree)
TEac (in hartree)
VIPS0 d (in eV)
VIPT1 e (in eV)
VEAS0 f(in eV)
VEAT1 g (in eV)
1263.668567 1263.681336 1263.699143
1263.420012 1263.468927 1263.496228
1263.713621 1263.757523 1263.803229
6.76 5.78 5.52
4.81 3.87 3.62
1.23 2.07 2.83
3.18 3.98 4.73
Total electronic energies of parent molecule. Total electronic energies of cation radical. Total electronic energies of anion radical. VIPS0 = TEcTEp. VIPT1 ¼ VIPS0 DET1 . VEAS0 = TEa TEp. VEAT1 ¼ VEAS0 DET1 .
the photosensitization of curcumin in benzene [11]. Thus, an alternative O2 -generating mechanism may exist. For instance, anion–cation radical couples of curcumin could be generated by redox reactions between T1 and S0 states (Eq. (3)) or both T1 states (Eq. (4)) of curcumin molecules. Then, the curcumin anion could pass its electron to the surrounding oxygen and generate O2 (Eq. (5)). The precondition for these reactions is that the total energy of each reaction is negative. CurðT1 Þ þ Cur ! Curþ þ Cur CurðT Þ þ CurðT Þ ! Curþ þ Cur
ð3Þ
Cur þ 3 O2 ! Cur þ O2
ð5Þ
1
1
ð4Þ
In benzene, the vertical electron affinity (VEA) for T1 state of curcumin ðVEAT1 Þ is 3.98 eV (Table 2), while the VIP for ground state ðVEAS0 Þ amounts to 5.78 eV (Table 2). The total energy of reaction (3) is positive and thus the reaction is forbidden. However, reaction (4) is permitted owing to its negative total reaction energy (VEAT1 (3.98 eV) + VIPT1 (3.87 eV) = 0.09 eV). In addition, since the total energy of reaction (5) is negative (AEAO2 (2.33 eV) VEAS0 (2.07 eV) = 0.26 eV), Cur can donate its excess electron to 3O2 to generate O2 (Eq. (5)). This accounts for the observed O2 -generating activity of curcumin in benzene. In DMSO, according to the calculated results (Table 2), reaction (3) is prohibited, while reactions (4) and (5) are allowed. Therefore, this O2 -generating pathway also exists in DMSO. Whereas in vacuum, judged from the present data (Table 2), both reactions (3) and (4) are forbidden, because of the positive reaction energies. Hence, O2 is unlikely generated in vacuum. In summary, TD-DFT-derived triplet excited-state properties of curcumin not only explained the experimentally observed photosensitizing features of curcumin, namely, both 1O2 and O2 can be generated in benzene and DMSO, but also revealed the difference in O2 -generating mechanisms in both solvents. Therefore, TD-DFT can serve as an efficient approach to determine triplet excited-state properties of photosensitizers both in vacuum and in solvents, by which one can get a deeper insight into the photodynamic mechanisms.
Acknowledgments This work was supported by the National Key Project for Basic Research (2003CB114400) and the National Natural Science Foundation of China (Grant No. 30100035).
References [1] O.P. Sharma, Biochem. Pharmacol. 25 (1976) 1811. [2] B. Vijayalaxmi, Mutat. Res. 79 (1980) 125. [3] B. Mishra, K.I. Priyadarsini, M.K. Bhide, R.M. Kadam, H. Mohan, Free Radical Res. 38 (2004) 355. [4] G. Litwinienko, K.U. Ingold, J. Org. Chem. 69 (2004) 5888. [5] A.J. Ruby, G. Kuttan, K.D. Babu, Cancer Lett. 94 (1995) 79. [6] B.B. Aggarwal, A. Kumar, A.C. Bharti, Anticancer Res. 23 (2003) 363. [7] M.E. Egan, M. Pearson, S.A. Weiner, V. Rajendran, D. Rubin, J. Gloo¨kner-Pagel, S. Canny, K. Du, G.L. Lukacs, M.J. Caplan, Science 304 (2004) 600. [8] E.S. Jankun, N.P. McCabe, S.H. Selman, J. Jankun, Int. J. Mol. Med. 6 (2000) 521. [9] N. Sreejayan, K.I. Priyadarsini, T.P.A. Devasagayam, M.N.A. Rao, Int. J. Pharm. 151 (1997) 125. [10] T.A. Dahl, P. Bilski, K.J. Reszka, C.F. Chignell, Photochem. Photobiol. 59 (1994) 290. [11] C.F. Chignell, P. Bilski, K.J. Reszka, A.N. Motten, R.H. Sik, T.A. Dahl, Photochem. Photobiol. 59 (1994) 295. [12] T.A. Dahl, W.M. McGowan, M.A. Shand, V.S. Srinivasan, Arch. Microbiol. 151 (1989) 183. [13] A.A. Gorman, V.S. Hamblett, V.S. Srinivasan, P.D. Wood, Photochem. Photobiol. 59 (1994) 389. [14] Y.-M. Sun, H.-Y. Zhang, D.-Z. Chen, C.-B. Liu, Org. Lett. 4 (2002) 2909. [15] J.S. Wright, J Mol. Struct. – Theochem. 591 (2002) 207. [16] L. Shen, H.-Y. Zhang, H.-F. Ji, Org. Lett. 7 (2005) 243. [17] R. Bauernschmitt, R. Ahlrichs, Chem. Phys. Lett. 256 (1996) 454. [18] F. Furche, J. Chem. Phys. 114 (2001) 5982. [19] M. Parac, S. Grimme, J. Phys. Chem. A 106 (2002) 6844. [20] M.J.S. Dewar, E.G. Zoebisch, E.F. Healy, J.J.P. Stewart, J. Am. Chem. Soc. 107 (1985) 3902. [21] R.E. Stratmann, G.E. Scuseria, M.J. Frisch, J. Chem. Phys. 109 (1998) 8218. [22] J. Llano, J. Raber, L.A. Eriksson, J. Photochem. Photobiol. A 154 (2003) 235. [23] S. Miertus, E. Scrocco, J. Tomasi, Chem. Phys. 55 (1981) 117. [24] S. Miertus, J. Tomasi, Chem. Phys. 65 (1982) 239.
L. Shen et al. / Chemical Physics Letters 409 (2005) 300–303 [25] M. Cossi, V. Barone, J. Cammi, Chem. Phys. Lett. 255 (1996) 327. [26] M.J. Frisch et al., GAUSSIAN 03, Gaussian, Inc., Pittsburgh, PA, 2003. [27] L.R.C. Barclay, M.R. Vinqvist, K. Mukai, Y. Hashimoto, A. Tokunaga, H. Uno, Org. Lett. 2 (2000) 2841.
303
[28] K.P. Huber, G. Herzberg, Molecular Spectra and Molecular Structure. Part IV. New York, 1979. [29] HJH. Fenton, J. Chem. Soc. 65 (1894) 889. [30] F. Haber, J. Weiss, Proc. Roy. Soc. Lond. Ser. A 147 (1934) 332.
A TD-DFT study on triplet excited-state properties of curcumin and its implications in elucidating the photosensitizing mechanisms of the pigment Liang Shen, Hong-Fang Ji, Hong-Yu Zhang
*
Shandong Provincial Research Center for Bioinformatic Engineering and Technique, Center for Advanced Study, Shandong University of Technology, Zhangzhou Road 12 #, Zibo 255049, PR China Received 21 March 2005; in final form 27 April 2005 Available online 8 June 2005
Abstract In this Letter, we present time-dependent density functional theory (TD-DFT)-derived triplet state properties of curcumin in vacuum, benzene and DMSO. Accordingly, the photosensitizing mechanisms of curcumin are explained. It is revealed that in benzene and DMSO, excited curcumin can react with O2 to generate 1O2 and O2 through energy transfer and electron transfer, however, the O2 -generating pathways are different in both solvents. This indicates the potential of TD-DFT in determining the excited-state properties of pigments, which is of significance in getting a deeper insight into the photodynamic mechanisms of photosensitizers. Ó 2005 Elsevier B.V. All rights reserved.
1. Introduction Curcumin [1,7-bis(4-hydroxy-3-methoxyphenyl)-1,6heptadiene-3,5-dione] is a yellow–orange pigment derived from the rhzone of Curcuma longa (Fig. 1A,B) [1,2], which has attracted considerable attention owing to its various significant biological activities, such as radical-scavenging activity, anticarcinogenic activity, antiinflammatory activity and phototoxicity [3–9]. Significant phototoxicity of curcumin against a variety of bacteria and viruses has made curcumin a potential photodynamic drug [10–12]. As the photosensitization of curcumin requires the presence of oxygen [10,12], reactive oxygen species (ROS) is very likely responsible for its phototoxicity. Although some experimental effort has been devoted to elucidating the photosensitive mechanisms of curcumin [11,13], no theoretical study has been performed on this topic, in sharp con*
Corresponding author. Fax: +86 533 278 0271. E-mail address: [email protected] (H.-Y. Zhang).
0009-2614/$ - see front matter Ó 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.cplett.2005.05.023
trast with the radical-scavenging mechanisms of curcumin, which have been intensively investigated by theoretical methods [14–16]. We think this partially results from the difficulty in the theoretical treatment of the short-lived excited-states of curcumin. Considering the successful use of time-dependent density functional theory (TD-DFT) in investigating the molecular excited-state properties [16–19], we attempt to explore the triplet excited-state properties of curcumin by means of TD-DFT, by which we will explain the photosensitive mechanisms of curcumin.
2. Methods Initial structures of curcumin-related compounds were optimized by semiempirical method AM1 [20]. Using these structures as starting points, the geometries were fully optimized by the hybrid B3LYP functional with 6-31G(d,p) Gaussian basis set. Finally, the triplet state properties were calculated by TD-DFT formalism
L. Shen et al. / Chemical Physics Letters 409 (2005) 300–303
301 H
CH3 O
O
O C H2
H
CH3 O
O
O H
O
O
CH3
CH3
O
O
C
H
H
H
O
O
curcumin (A)
curcumin (B) Fig. 1. Molecular structure of curcumin.
with the same basis set [21]. This method has been justified by the calculation of absorption spectrum of curcumin that the method precisely predicts the absorption peak of the pigment [16]. In addition, as the diffusion functions are essential for the treatment of anion and cation radicals, the electron affinities and ionization potentials of curcumin were calculated by a combined method B3LYP/6-31G+(d,p)//B3LYP/6-31G(d,p) [22], which means that B3LYP/6-31G+(d,p) was employed to do a single-point calculation on the basis of B3LYP/ 6-31G(d,p)-optimized structures. During the calculation, both in vacuo and in solvent models were considered. The solvent (benzene and DMSO) effects were involved by employing the self-consistent reaction field (SCRF) method with polarized continuum model (PCM) [23–25]. For molecular oxygen-related parameters, B3LYP/631G+(d,p) was employed to do full-geometry-optimization calculation. All of the calculations were performed with GAUSSIAN 03 package of programs [26].
3. Results and discussion Although curcumin exists in two conformations, A and B (Fig. 1), B predominates in various solvents [13,27], which has also been proved by our theoretical studies [14,16]. Hence, curcumin B is used as starting point of calculation. As it is the triplet state that is responsible for the photosensitizing activity, we focused our study on triplet excited-state of curcumin. 3.1. T1 transition energy Since the lowest T1 transition energy ðDET1 Þ of a photosensitizer is crucial to understanding the photosensitizing mechanisms, we calculated the DET1 of curcumin at first. The DET1 of curcumin in vacuum, benzene and DMSO, 1.95, 1.91 and 1.90 eV (Table 1), are similar
Table 1 The lowest T1 transition energy of curcumin (in eV) DET1
Vacuum
Benzene
DMSO
1.95
1.91
1.90
to one another, indicating that DET1 is slightly influenced by environment. In addition, it is interesting to note that the theoretical DET1 in benzene is close to the experimental value (1.98 eV) [13]. As it is still a challenge to determine DET1 by experiments, the theoretical method seems a proper alternative approach to estimate DET1 of photosensitizers. The DET1 of curcumin is higher than the excited-state energy of singlet oxygen (1O2), 1.06 eV [22], suggesting that curcumin can, in principle, generate 1O2 through energy transfer (Eq. (1)), which agrees well with the experimental finding that curcumin gives birth to 1O2 in benzene with a yield of 0.12 [13]. CurðT1 Þ þ 3 O2 ! CurðS0 Þ þ 1 O2
ð1Þ
3.2. Vertical ionization potential and vertical electron affinity of T1 state Besides energy transfer, photosensitizer also can donate an electron to oxygen and generate superoxide anion radical ðO2 Þ (Eq. (2)). The prerequisite of the reaction is that the summation of vertical ionization potential (VIP) for T1 state (VIPT1) of the pigment and the adiabatic electron affinity (AEA) of molecular oxygen (3O2) is negative. ð2Þ CurðT Þ þ 3 O ! Curþ þ O 1
2
2
In vacuum, the AEA of 3O2 was calculated to be 0.59 eV, which can be compared with the experimental value, 0.45 eV [28]. Whereas, the in vacuo VIPT1 of curcumin was estimated to be 4.81 eV (Table 2), implying that curcumin on T1 state could not donate an electron to oxygen in this case. While in DMSO, the AEA of 3 O2 was calculated to be 3.65 eV and the VIPT1 of curcumin became 3.62 eV (Table 2). Therefore, the O2 can be generated in DMSO by photosensitization of curcumin, which is consistent with the experimental observation [11]. Once O2 is given, other ROS, such as H2O2 and OH can be produced through Fenton reaction [29] or Haber–Weiss reaction [30], which will efficiently amplify the photosensitizing activity of curcumin. In benzene, the AEA of O2 was calculated as 2.33 eV and the VIPT1 of curcumin was 3.87 eV (Table 2), suggesting that O2 could not be generated through this pathway. However, O2 is indeed observed during
302
L. Shen et al. / Chemical Physics Letters 409 (2005) 300–303
Table 2 The vertical ionization potentials (VIPs, in eV) and vertical electron affinities (VEAs, in eV) of curcumin in S0 and T1 states Vacuum Benzene DMSO a b c d e f g
TEpa (in hartree)
TEcb (in hartree)
TEac (in hartree)
VIPS0 d (in eV)
VIPT1 e (in eV)
VEAS0 f(in eV)
VEAT1 g (in eV)
1263.668567 1263.681336 1263.699143
1263.420012 1263.468927 1263.496228
1263.713621 1263.757523 1263.803229
6.76 5.78 5.52
4.81 3.87 3.62
1.23 2.07 2.83
3.18 3.98 4.73
Total electronic energies of parent molecule. Total electronic energies of cation radical. Total electronic energies of anion radical. VIPS0 = TEcTEp. VIPT1 ¼ VIPS0 DET1 . VEAS0 = TEa TEp. VEAT1 ¼ VEAS0 DET1 .
the photosensitization of curcumin in benzene [11]. Thus, an alternative O2 -generating mechanism may exist. For instance, anion–cation radical couples of curcumin could be generated by redox reactions between T1 and S0 states (Eq. (3)) or both T1 states (Eq. (4)) of curcumin molecules. Then, the curcumin anion could pass its electron to the surrounding oxygen and generate O2 (Eq. (5)). The precondition for these reactions is that the total energy of each reaction is negative. CurðT1 Þ þ Cur ! Curþ þ Cur CurðT Þ þ CurðT Þ ! Curþ þ Cur
ð3Þ
Cur þ 3 O2 ! Cur þ O2
ð5Þ
1
1
ð4Þ
In benzene, the vertical electron affinity (VEA) for T1 state of curcumin ðVEAT1 Þ is 3.98 eV (Table 2), while the VIP for ground state ðVEAS0 Þ amounts to 5.78 eV (Table 2). The total energy of reaction (3) is positive and thus the reaction is forbidden. However, reaction (4) is permitted owing to its negative total reaction energy (VEAT1 (3.98 eV) + VIPT1 (3.87 eV) = 0.09 eV). In addition, since the total energy of reaction (5) is negative (AEAO2 (2.33 eV) VEAS0 (2.07 eV) = 0.26 eV), Cur can donate its excess electron to 3O2 to generate O2 (Eq. (5)). This accounts for the observed O2 -generating activity of curcumin in benzene. In DMSO, according to the calculated results (Table 2), reaction (3) is prohibited, while reactions (4) and (5) are allowed. Therefore, this O2 -generating pathway also exists in DMSO. Whereas in vacuum, judged from the present data (Table 2), both reactions (3) and (4) are forbidden, because of the positive reaction energies. Hence, O2 is unlikely generated in vacuum. In summary, TD-DFT-derived triplet excited-state properties of curcumin not only explained the experimentally observed photosensitizing features of curcumin, namely, both 1O2 and O2 can be generated in benzene and DMSO, but also revealed the difference in O2 -generating mechanisms in both solvents. Therefore, TD-DFT can serve as an efficient approach to determine triplet excited-state properties of photosensitizers both in vacuum and in solvents, by which one can get a deeper insight into the photodynamic mechanisms.
Acknowledgments This work was supported by the National Key Project for Basic Research (2003CB114400) and the National Natural Science Foundation of China (Grant No. 30100035).
References [1] O.P. Sharma, Biochem. Pharmacol. 25 (1976) 1811. [2] B. Vijayalaxmi, Mutat. Res. 79 (1980) 125. [3] B. Mishra, K.I. Priyadarsini, M.K. Bhide, R.M. Kadam, H. Mohan, Free Radical Res. 38 (2004) 355. [4] G. Litwinienko, K.U. Ingold, J. Org. Chem. 69 (2004) 5888. [5] A.J. Ruby, G. Kuttan, K.D. Babu, Cancer Lett. 94 (1995) 79. [6] B.B. Aggarwal, A. Kumar, A.C. Bharti, Anticancer Res. 23 (2003) 363. [7] M.E. Egan, M. Pearson, S.A. Weiner, V. Rajendran, D. Rubin, J. Gloo¨kner-Pagel, S. Canny, K. Du, G.L. Lukacs, M.J. Caplan, Science 304 (2004) 600. [8] E.S. Jankun, N.P. McCabe, S.H. Selman, J. Jankun, Int. J. Mol. Med. 6 (2000) 521. [9] N. Sreejayan, K.I. Priyadarsini, T.P.A. Devasagayam, M.N.A. Rao, Int. J. Pharm. 151 (1997) 125. [10] T.A. Dahl, P. Bilski, K.J. Reszka, C.F. Chignell, Photochem. Photobiol. 59 (1994) 290. [11] C.F. Chignell, P. Bilski, K.J. Reszka, A.N. Motten, R.H. Sik, T.A. Dahl, Photochem. Photobiol. 59 (1994) 295. [12] T.A. Dahl, W.M. McGowan, M.A. Shand, V.S. Srinivasan, Arch. Microbiol. 151 (1989) 183. [13] A.A. Gorman, V.S. Hamblett, V.S. Srinivasan, P.D. Wood, Photochem. Photobiol. 59 (1994) 389. [14] Y.-M. Sun, H.-Y. Zhang, D.-Z. Chen, C.-B. Liu, Org. Lett. 4 (2002) 2909. [15] J.S. Wright, J Mol. Struct. – Theochem. 591 (2002) 207. [16] L. Shen, H.-Y. Zhang, H.-F. Ji, Org. Lett. 7 (2005) 243. [17] R. Bauernschmitt, R. Ahlrichs, Chem. Phys. Lett. 256 (1996) 454. [18] F. Furche, J. Chem. Phys. 114 (2001) 5982. [19] M. Parac, S. Grimme, J. Phys. Chem. A 106 (2002) 6844. [20] M.J.S. Dewar, E.G. Zoebisch, E.F. Healy, J.J.P. Stewart, J. Am. Chem. Soc. 107 (1985) 3902. [21] R.E. Stratmann, G.E. Scuseria, M.J. Frisch, J. Chem. Phys. 109 (1998) 8218. [22] J. Llano, J. Raber, L.A. Eriksson, J. Photochem. Photobiol. A 154 (2003) 235. [23] S. Miertus, E. Scrocco, J. Tomasi, Chem. Phys. 55 (1981) 117. [24] S. Miertus, J. Tomasi, Chem. Phys. 65 (1982) 239.
L. Shen et al. / Chemical Physics Letters 409 (2005) 300–303 [25] M. Cossi, V. Barone, J. Cammi, Chem. Phys. Lett. 255 (1996) 327. [26] M.J. Frisch et al., GAUSSIAN 03, Gaussian, Inc., Pittsburgh, PA, 2003. [27] L.R.C. Barclay, M.R. Vinqvist, K. Mukai, Y. Hashimoto, A. Tokunaga, H. Uno, Org. Lett. 2 (2000) 2841.
303
[28] K.P. Huber, G. Herzberg, Molecular Spectra and Molecular Structure. Part IV. New York, 1979. [29] HJH. Fenton, J. Chem. Soc. 65 (1894) 889. [30] F. Haber, J. Weiss, Proc. Roy. Soc. Lond. Ser. A 147 (1934) 332.