Letter pubs.acs.org/JPCL
Dissociative Electron Attachment to Resveratrol as a Likely Pathway for Generation of the H2 Antioxidant Species Inside Mitochondria Stanislav A. Pshenichnyuk*,†,‡ and Alexei S. Komolov‡ †
Institute of Molecule and Crystal Physics, Ufa Research Centre, Russian Academy of Sciences, Prospeκt Oktyabrya 151, 450075 Ufa, Russia ‡ Physics Faculty, St. Petersburg State University, Uljanovskaja 1, 198504 St. Petersburg, Russia ABSTRACT: The electron-attaching properties of polyphenolic compound resveratrol were studied in vacuo by means of dissociative electron attachment (DEA) spectroscopy and in silico using density functional theory calculations. The most intense fragments generated by DEA to isolated resveratrol at thermal electron energy are semiquinone anions and neutral hydrogen molecules. On the basis of the present experimental and theoretical data, a new molecular mechanism for the antioxidant activity of resveratrol is presented. It is suggested that the activity of resveratrol in living cells is driven by dissociative attachment of electrons “leaked” from the respiratory chain to this polyphenolic molecule, followed by the formation of the H2 antioxidant species inside mitochondria and participation in mitochondrial energy biogenesis.
R
with extra electrons under reductive conditions in cells. This type of interaction can occur in the vicinity of the pathway of electron transport in mitochondria provided that the electron affinity of the antioxidant species is comparable to that of molecular oxygen.7 The dissociative electron attachment (DEA) reaction with multiple OH-substituted aromatic compounds has been found to efficiently produce doubly dehydrogenated (semiquinone) anions and H2 neutral species.5,8 Recently, H2 gas has been found to be the simplest antioxidant species and has been successfully used clinically with a series of delivery methods.9−11 The present Letter reports a new molecular mechanism of the antioxidant activity of the polyphenolic compound resveratrol. This mechanism is linked to the possibility of xenobiotic species to be reduced in the mitochondrial intermembrane space with electrons “leaked” from Complex III of the respiratory chain. This possibility has been recently demonstrated, for example, with anthralin, an antipsoriatic drug extensively active in the mitochondria of keratinocytes.8 Our hypothesis suggests that the generation of neutral H2 molecules inside the intermembrane space, in other words, at a site where the native antioxidant system is weaker than that in the mitochondrial matrix,12 is likely to involve DEA with polyphenolic compounds. Therefore, this mechanism can provide protection against mitochondrial damage caused by reactive oxygen species (ROS) under oxidative stress conditions or via exposure of a living organism to toxic xenobiotic species, as has been
esveratrol (3,4′,5-trihydroxystilbene; see Chart 1), a naturally occurring plant phytoalexin and a well-known
Chart 1. Molecular Structure of trans-Resveratrol and the Atom Labeling
constituent of red wine, has strong antioxidant effects and has been reported to possesses beneficial effects on human health by preventing a wide variety of illnesses, for example, cancer, cardiovascular malfunction, neurodegenerative diseases, inflammation, and atherosclerosis;1−3 however, the molecular mechanism of action of resveratrol resulting in this variety of beneficial effects is not yet known.1 In general, the useful effects of natural polyphenolic compounds are associated with their antioxidant properties, and two main mechanisms of scavenging of free radicals are under consideration.4 The first one is attributed to H-atom abstraction from hydroxyl groups and transfer to reactive species to interrupt the chain reaction of lipid peroxidation, governed by the rate of OH bond cleavage. The second mechanism is associated with electron removal from antioxidant molecules to form radical cations, followed by rapid deprotonation, which is governed by the ionization potential. Some polyphenolic antioxidants, such as flavonoids and spinochromes, are good electron acceptors5,6 and can interact © 2015 American Chemical Society
Received: February 20, 2015 Accepted: March 11, 2015 Published: March 11, 2015 1104
DOI: 10.1021/acs.jpclett.5b00368 J. Phys. Chem. Lett. 2015, 6, 1104−1110
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The Journal of Physical Chemistry Letters
Figure 1. Mass-selected currents of negative ions formed by DEA to gas-phase resveratrol as a function of incident electron energy (left panel). Schematic view of dissociative pathways of the resveratrol temporary negative ion in vacuo (right panel). The thickness of the red arrows is approximately proportional to the integral intensity of the corresponding pathway.
= 0.8065 × VOE + 0.9194), derived for the π* molecular orbitals (MOs) of alternating phenyl and ethynyl groups,24 was employed to scale the B3LYP/6-31G(d) π* VOEs. The first vertical electron affinity was calculated as the difference between the total energy (only electronic contributions) of the neutral state and the lowest anion state, both in the optimized geometry of the neutral state, using the standard 6-31+G(d) basis set with the minimum addition of diffuse functions. The adiabatic electron affinity (EAa) was obtained as the energy difference between the neutral state and the lowest anion state, each in its optimized geometry. The thermodynamic energy thresholds for the formation of fragments by DEA were evaluated as the difference between their total energy and that of the neutral ground state. The effects of the solvated environment were evaluated using the polarizable continuum model (PCM).25 Isolated resveratrol molecules can efficiently attach lowenergy electrons in vacuo, producing five negatively charged species with mass numbers (m/e) 225−228 and 185, as detected by our apparatus. The currents of these negative ions as a function of incident electron energy are presented in Figure 1; their likely structures, peak energies and relative intensities are listed in Table 1. The most intense signal peaked at 1.2 eV
discussed for a series of pesticides.13 The generation of lipid peroxidizing radicals in the intermembrane space could lead to the disruption of either the outer or inner mitochondrial membrane. In the former case, cytochrome c can be released from damaged mitochondria into the cytosol, thus signaling the cell to undergo apoptosis. In the latter case, the broken inner membrane provides access for free radicals to the mitochondrial matrix and its DNA, potentially leading to genetic mutations. The present investigation may shed some light on the mechanism of biochemical reactions under reductive conditions and the therapeutic effects of polyphenolic compounds. Low-energy electron attachment to resveratrol was investigated by DEA spectroscopy.14,15 Our magnetic mass spectrometer has previously been described in detail.16 In brief, a magnetically collimated electron beam of defined energy was passed through a collision cell containing a vapor of the substance under investigation, under single-collision conditions. A signal for the mass-selected negative ions was recorded as a function of the incident electron energy in the 0−14 eV energy range. The electron-energy scale was calibrated with the SF6− signal at zero energy, generated by the attachment of thermal electrons to SF6. The full width at half-maximum (fwhm) of the electron-energy distribution was 0.4 eV, and the accuracy of the measured peak positions was estimated to be ±0.1 eV. Resveratrol powder (Sigma-Aldrich no. R5010) was evaporated at 170 °C, and the collision cell was held 10 °C higher to prevent condensation. The experimental features were interpreted with the support of density functional theory (DFT) calculations, performed using the Gaussian 09 program package.17 The virtual orbital energies (VOEs) of the neutral molecules were evaluated using the B3LYP18 hybrid functional with the standard 6-31G(d) basis set. It has been demonstrated19,20 that good linear correlations can be obtained between the experimental vertical attachment energies (VAEs) and the corresponding VOEs for neutral molecules calculated with basis sets that do not include diffuse functions. The scaling procedure was successfully used for the peak assignment of the experimentally obtained density of the unoccupied states in small conjugated molecular materials.21−23 In the present study, the linear equation (VAE
Table 1. Probably Structures of Fragment Negative Ions Observed in DEA Spectrum of Resveratrol, Peak Energies (eV), and Relative Intensities Evaluated from the Peak Heightsa m/e
a
1105
anion structure
228 227
M− [M − H]−
226
[M − 2H]−
225
[M − 3H]−
185
[M − (CH)2OH]−
peak energy 0.0 1.2 4.3 0.0 0.6 sh. 4.5 9.5 8.7
relative intensity 45 100 24 17 0.8 1.3 0.8
M stands for resveratrol; sh. stands for shoulder. DOI: 10.1021/acs.jpclett.5b00368 J. Phys. Chem. Lett. 2015, 6, 1104−1110
Letter
The Journal of Physical Chemistry Letters
Table 2. B3LYP/6-31+G(d) Total Energies (eV) Relative to the Neutral Ground State of Resveratrol in the Gas Phase and in Watera relative energy
a
no.
m/e
fragments
gas phase
water
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
228 228 227 227 227 227 227 226 226 226 226 226 226 225 225 225 185 185
vertical M− adiabatic M− [M − H(4′)]− + H [M − H(5)]− + H [M − H(3)]− + H [M − H(4)]− + H [M − H(7)]− + H [M − 2H(4′,5)]− + H2 [M − 2H(3,4′)]− + H2 [M − 2H(3,5)]− + H2 [M − 2H(2,2′)]− + H2 [M − 2H(7,8)]− + H2 [M − 2H(4,5)]− + H2 [M − 3H(2,2′,3)]− + H2 + H [M − 3H(3,4,5)]− + H2 + H [M − 3H(3,4′,5)]− + H2 + H [M − (CH)2OH(3)]− + COCH3 [M − (CH)2OH(4′)]− + COCH3
−0.33 −0.54 0.62 0.98 0.96 2.67 2.74 −0.93 −0.93 −0.55 −0.37 1.19 1.80 0.46 2.41 2.77 5.04 5.28
−2.02 −2.20 −1.21 −1.10 −1.10 0.63 0.88 −2.61 −2.62 −2.57 −1.99 −0.49 −0.55 −1.42 0.59 1.08 3.06 3.18
(1) (2) (3) (4) (5) (6) (7) (8) (9) (10)
Numbering labels refer to the structures reported in Chart 2; values include zero-point vibrational energy corrections.
Chart 2. Structures of the Fragment Negative Ions
with a second peak at 4.3 eV (see Figure 1 and Table 1), attributed to the formation of dehydrogenated [M−H]− species (m/e = 227). Table 2 reports the B3LYP/6-31+G(d) thermodynamic energy thresholds for the formation of fragments by DEA. According to the present calculation (line nos. 3−7 in Table 2), the lowest energy threshold (0.62 eV) was predicted for H-atom abstraction from the 4′ site (see Chart 1), although C(3)−H or C(5)−H bond breakage (the corresponding thresholds are nearly equal to each other) can also be responsible for the m/e = 227 signal at 1.2 eV. H-atom elimination from positions 4 and 7 was predicted to be possible above 2.5 eV and may account for the second peak at 4.3 eV in the m/e = 227 current.
The EAa of resveratrol was estimated to be 0.54 eV (line no. 2 in Table 2); this is high enough to allow for the observation of long-lived (microseconds, i.e., mass spectrometrically detectable) molecular negative ions M− (m/e = 228) at thermal electron energy. (The peak at 4.3 eV is ascribed to the isotopic contribution of the m/e = 227 signal.) However, the calculated EAa could be somewhat overestimated; for comparison, the EAa for trans-stilbene calculated by the same procedure is 0.55 eV, whereas its experimental value is 0.35 eV.26 The formation of M− at zero energy is in competition with the dissociative process observed at the same energy that leads to the formation of doubly dehydrogenated [M−2H]− species (m/e = 226). The process is expected to be exothermic, provided that two H atoms are eliminated from the (4′,5), 1106
DOI: 10.1021/acs.jpclett.5b00368 J. Phys. Chem. Lett. 2015, 6, 1104−1110
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The Journal of Physical Chemistry Letters (3,4′), and (3,5) sites (line nos. 8−10 in Table 2), leading to the formation of the CO double bonds (structures 1−3 in Chart 2). The other requirement is that the H2 molecule must be formed as a neutral counterpart. Despite the higher energy benefit, abstraction of two H atoms from the (4′,5) and (3,4′) sites requires H-atom migration along the entire molecule to form the neutral H2 species and is therefore less probable. The most likely structure of the [M−2H]− fragment in vacuo is expected to be (3,5)-semiquinone (structure 3 in Chart 2); however, quinone structures 1 and 2 cannot be completely ruled out. Abstraction of two hydrogen atoms from the (2,2′) sites (more likely to occur in cis-resveratrol) can also lead to stable products (line no. 11 in Table 2) provided that one more aromatic ring is formed, to give an [M−2H]− anion with the 3,5,7-trihydroxy-phenanthrene structure (structure 4 in Chart 2). A possibility offered by the stilbene structure is the removal of two hydrogen atoms from the CC bridge to form a triple bond (structure 5 in Chart 2); the energy threshold (1.19 eV) predicted by the calculations, however, indicates that this process cannot contribute to the m/e = 226 signals observed at low energy. If one H atom is taken from the aromatic ring, the formation of [M−2H]− is also predicted to be endothermic (line no. 13 in Table 2) and can only account for a very small (not reported in Table 1) signal in the m/e = 226 current around 4 and 6 eV. Elimination of three H atoms (m/e = 225) was observed at high incident electron energy in line with predicted thresholds (line nos. 14−16 in Table 2). Structure 6 reported in Chart 2 corresponds to the removal of one H atom from the phenanthrene structure 4 and requires only 0.5 eV to be formed, but the signal was not observed at low energy. (See Figure 1.) Structure 7 is strongly rearranged but is slightly more stable than structure 8. Finally, the disruption of one aromatic ring in the resveratrol anion can lead to the elimination of a CH3CO• neutral radical from M−, producing a negatively charged species with m/e = 185. The predicted threshold exceeds 5 eV; this is in line with the observation of a very broad signal of this negative fragment peaking at 8.7 eV which appears only above 5 eV. (See Figure 1.) A summary of the fragmentation scheme of resveratrol by DEA in vacuo is reported in Figure 1. DEA reactions depicted in Figure 1 are initiated by resonant formation of negative ion states via the addition of an extra electron to neutral resveratrol. The energies of vertical formation of the negative ion states were evaluated by scaling the B3LYP/6-31G(d) VOEs with an empirical linear equation, and the predicted VAEs are reported in Table 3. Whereas its adiabatic negative ion is predicted to be planar, the optimized neutral state structure of trans-resveratrol is predicted to be slightly “twisted” (Figure 2a), in line with a gas-phase electron diffraction study of the reference compound trans-stilbene.27 According to the present calculations, cis-resveratrol possesses a “propeller-like” structure (Figure 2b) and is 0.2 eV less stable than trans-resveratrol. We thus consider only the trans isomer. A schematic view of resveratrol π* orbitals whose contribution to DEA is usually stronger than that of more short-lived σ* states28 is reported in Figure 2c. This Figure also reports the resonance energies predicted by the scaling procedure. The empty π* orbitals possess mainly benzene character, although the π4* and π5* MOs have large contributions from the CC ethene double bond. The reliability of the VAEs predicted by the scaling procedure is
Table 3. B3LYP/6-31G(d) VOEs and Predicted Positions of Negative Ion Resonances (VAEs) and Experimental VAEs for trans-Stilbene29a resveratrol
stilbene
orbital
VOE
predict. VAE
VOE
predict. VAE
expt. VAE
π7* π6* π5* π4* π3* π2* π1*
5.211 4.743 2.322 0.734 0.660 −0.097 −1.201
5.12 4.74 2.79 1.51 1.45 0.84 −0.05
5.047 4.559 2.103 0.486 0.053 0.036 −1.357
5.00 4.60 2.61 1.31 0.96 0.95 −0.18
5.03 4.37 2.56 1.43
a
0.86
All values are in electronvolts.
supported by the very good match supplied by the same method with the VAEs measured29 in the reference molecule stilbene. The lowest unoccupied MO of resveratrol is predicted to be somewhat stable (see Table 3), which is in line with the predicted vertical electron affinity (line no. 1 in Table 2). Electron attachment to this MO gives rise to a vibrational Feshbach resonance14,15,28 responsible for the observation of zero-energy signals (m/e = 226, 228 in Figure 1). The most intense signal (m/e = 227) peaks at 1.2 eV and is associated with the unresolved contributions of the π3* and π4* shape resonances,28 very close in energy to each other. The small shoulder at 0.6 eV in the m/e = 226 signal could arise from electron addition to the π2* MO with a predicted VAE of 0.84 eV. The π5* and π7* MOs have no distinct counterparts in the DEA spectra, probably due to fast electron detachment from temporary anions formed at relatively high energies. Although the π6* MO (predicted VAE 4.74 eV) could be associated with the 4.3 and 4.5 eV signals observed in the m/e = 227 and 225 curves, respectively, these states are expected to be mixed with more long-lived core-excited resonances.14,28 Indeed, the experimental excitation energy of the lowest triplet transition in the reference trans-stilbene was detected at 2.1 to 2.2 eV.30 Core-excited states may also be responsible for higher energy signals at m/e = 225 and 185. Strong stabilization (about 1.7 to 2.0 eV) of negative ion states is predicted by the present PCM calculations, going from the gas phase to water solution (last column of Table 3). This finding implies that the formation of fragment negative ions by DEA to solvated resveratrol should be possible under ambient water (which in turn models the conditions in living cells) by capture of presolvated31 or even a portion (possessing high energy) of solvated electrons.8 In addition to the energy stabilization due to the solvent effect,32,21,22 the DEA crosssection is predicted to increase by one to two orders of magnitude when electron attachment occurs in water clusters.33 Because [M−2H]− is formed at a much lower energy than [M− H]− (thermal energy against 1.2 eV; see Table 1) and the energy benefits from the former DEA process is much higher than that in the latter (the difference is >1.5 eV; compare Table 2 line nos. 3 and 8), this leads to the conclusion that formation of the [M−2H]− species could become the dominant DEA decay in solution. The most likely structure of the fragments for both energetic (energy benefits) and kinetic (small rearrangements) reasons should be semiquinone structure 3 (Chart 2) and a neutral H2 molecule. Although one H-atom abstraction from the 4′ position (structures 1 and 2 in Chart 2) is expected to produce more energy benefit, this requires migration for a 1107
DOI: 10.1021/acs.jpclett.5b00368 J. Phys. Chem. Lett. 2015, 6, 1104−1110
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Figure 2. B3LYP/6-31+G(d)-optimized neutral-state geometry of (a) trans- and (b) cis-resveratrol. (c) Schematic view of B3LYP/6-31G(d) vacant π* MOs of neutral trans-resveratrol and expected positions (scaled VOEs) of the corresponding negative ion states in vacuo (vertical bars).
longer distance to form the H2 species. In fact, semiquinone anions of polyphenolic flavonoids have been found to be efficiently generated by electrospray ionization collisioninduced dissociation, the process being associated with the presence of catechol moiety.34 The protonation rate of semiquinone anions of hydroquinone and catechol in aqueous solution has been found to be strongly dependent on the pH.35 Being an effective antioxidant, resveratrol must possess activity inside mitochondria as it is the main site of ROS production in cells. Indeed, resveratrol has been found to influence processes in mitochondria and modulates their function via an increase in mitochondrial biogenesis; however, the exact molecular mechanism is unknown.36,37 The present mechanism of resveratrol activity is based on the idea that it can penetrate into the mitochondrial intermembrane space and interact with quasi-free electrons “leaked” from Complex III of the respiratory chain.38 This possibility for xenobiotic molecules as well as the relation of gas-phase DEA data to a cellular environment have been extensively discussed elsewhere.8,13,16,31 The estimated EAa of resveratrol (0.54 eV) is comparable to that of O2 (0.45 eV39), so it can compete7 with cellular oxygen for electrons leaked from Complex III, as indicated in Figure 3. According to the conclusion of the previous section (which is in line with the present in vacuo and in silico data), the main species generated by the hypothetical interaction of mitochondrial electron with resveratrol in the intermembrane space in vivo are expected to be (i) semiquinone [M − 2H]− and (ii) a neutral H2 molecule. (See Figure 3.) Since the recent publication of a pioneering study9 highlighting the role of H2 as a selective antioxidant, its ability to scavenge free radicals and its application as a therapeutic medical gas have been intensively studied. (For reviews, see refs 10 and 11.) It was found that hydrogen treatment via inhalation or intake of hydrogen-rich water is a very promising strategy to combat a variety of diseases9 because H2 can selectively scavenge very active hydroxyl radicals and peroxynitrite but does not eliminate superoxide, H2O2, or nitric oxide, thus sparing the innate immune system.10,11 Turning back to the present consideration, it should be noted that the generation of H2 by DEA to resveratrol in mitochondria (see Figure 3) would
Figure 3. Schematic representation of the likely resveratrol activity in the intermembrane space: formation of a temporary negative ion by the attachment of “leaked” electrons (analogously to superoxide formation), followed by the generation of the [M − 2H] − semiquinone and the neutral H2 radical scavenger via the DEA mechanism in vivo.
be an efficient and natural pathway to deliver this simple antioxidant to the site of ROS generation to deactivate the most toxic OH• and ONOO− species. Because cellular resveratrol is expected to compete with O2 for “leaked” electrons, it additionally prevents the formation of ROS initiated by the generation of superoxide anions. The negatively charged [M − 2H]− fragment possessing a semiquinone structure is the other product of the hypothetical DEA to resveratrol in vivo. It can serve as an electron carrier, thus returning the “leaked” electron back to the respiration chain and therefore participating in mitochondrial energy biogenesis and producing a beneficial effect in the cell. This hypothesis is in line with the reported conversion of αtocopherol to its quinone form by respiratory oxidative stress in vivo.40 The quinone tocopherol content has been found to be higher in the rat liver mitochondrial inner membrane than in the outer membrane, thus suggesting its role as an electron carrier species.40 The quinone form of resveratrol has not yet 1108
DOI: 10.1021/acs.jpclett.5b00368 J. Phys. Chem. Lett. 2015, 6, 1104−1110
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The Journal of Physical Chemistry Letters been identified, probably due to difficulties in its isolation,41 whereas the ortho-quinone form of polyphenolic quercetin, formed by 2H removal from its catechol motif, has been identified among its metabolites.42 This finding is in agreement with the observed DEA-stimulated formation of doubly dehydrogenated anions in quercetin5 as well as with Palladin’s hypothesis on the involvement of the quinone form of polyphenolic compounds in respiration in plants.43 In conclusion, the physiological activity of exogenous compounds is usually complex and multifaceted, and, in particular, resveratrol should act through multiple pathways. Nevertheless, the present mechanism of antioxidant activity could be applicable to other polyphenolic compounds and takes into account the number of OH groups and their relative positions. Qualitatively, multiple hydroxyl substitutions and neighboring sites of OH groups will increase the DEA crosssection and promote the elimination of two H atoms as a hydrogen molecule. The present mechanism reduces the variety of beneficial effects produced by polyphenolic antioxidants on health to the radical-scavenging ability of one simple species, the H2 molecule. These data may shed some light on mitochondrial processes important in the promising field of mitochondrial medicine.44 The most crucial point of the present mechanism is the fate of the temporary molecular negative ion formed in the cellular environment by quasi-free electron attachment: whether it will dissipate its excess energy to the surrounding media and thus escape dissociation32 or, conversely, whether neighboring water molecules will increase33 the DEA cross-section and stimulate H atom abstraction from it.
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(7) Biaglow, J. E. Cellular Electron Transfer and Radical Mechanisms for Drug Metabolism. Radiat. Res. 1981, 86, 212−242. (8) Pshenichnyuk, S. A.; Komolov, A. S. Dissociative Electron Attachment to Anthralin to Model Its Biochemical Reactions. J. Phys. Chem. Lett. 2014, 5, 2916−2921. (9) Ohsawa, I.; Ishikawa, M.; Takahashi, K.; Watanabe, M.; Nishimaki, K.; Yamagata, K.; Ken-ichiro Katsura, K.; Katayama, Y.; Asoh, S.; Ohta, S. Hydrogen Acts as a Therapeutic Antioxidant by Selectively Reducing Cytotoxic Oxygen Radicals. Nat. Med. 2007, 13, 688−694. (10) Huang, C. S.; Kawamura, T.; Toyoda, Y.; Nakao, A. Recent Advances in Hydrogen Research as a Therapeutic Medical Gas. Free Radical Res. 2010, 44, 971−982. (11) Hong, Y.; Chen, S.; Zhang, J. M. Hydrogen as a Selective Antioxidant: A Review of Clinical and Experimental Studies. J. Int. Med. Res. 2010, 38, 1893−1903. (12) Andreyev, A. Y.; Kushnareva, Y. E.; Starkov, A. A. Mitochondrial Metabolism of Reactive Oxygen Species. Biochemistry (Moscow) 2005, 70, 200−214. (13) Pshenichnyuk, S. A.; Modelli, A. Can Mitochondrial Dysfunction be Initiated by Dissociative Electron Attachment to Xenobiotics? Phys. Chem. Chem. Phys. 2013, 15, 9125−9135. (14) Allan, M. Study of Triplet States and Short-Lived Negative Ions by Means of Electron Impact Spectroscopy. J. Electron Spectrosc. Relat. Phenom. 1989, 48, 219−351. (15) Illenberger, E.; Momigny, J. Gaseous Molecular Ions. An Introduction to Elementary Processes Induced by Ionization; SpringerVerlag: New York, 1992. (16) Pshenichnyuk, S. A.; Modelli, A.; Weissig, V.; Edeas, M. ETS and DEAS Studies of the Reduction of Xenobiotics in Mitochondrial Intermembrane Space. Methods Mol. Biol. (N. Y., NY, U. S.) 2015, 1265, 285−305. (17) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; et al. Gaussian 09, revision A.02; Gaussian, Inc.: Wallingford, CT, 2009. (18) Becke, A. D. Density-Functional Thermochemistry. III. The Role of Exact Exchange. J. Chem. Phys. 1993, 98, 5648−5652. (19) Chen, D.; Gallup, G. A. The Relationship of the Virtual Orbitals of Self-Consistent-Field Theory to Temporary Negative Ions in Electron Scattering from Molecules. J. Chem. Phys. 1990, 93, 8893− 8901. (20) Modelli, A. Electron Attachment and Intramolecular Electron Transfer in Unsaturated Chloroderivatives. Phys. Chem. Chem. Phys. 2003, 5, 2923−2930. (21) Pshenichnyuk, S. A.; Komolov, A. S. Relation between Electron Scattering Resonances of Isolated NTCDA Molecules and Maxima in the Density of Unoccupied States of Condensed NTCDA Layers. J. Phys. Chem. A 2011, 116, 761−766. (22) Pshenichnyuk, S. A.; Kukhto, A. V.; Kukhto, I. N.; Komolov, A. S. Spectroscopic States of PTCDA Negative Ions and Their Relation to the Maxima of Unoccupied State Density in the Conduction Band. Technol. Phys. 2011, 56, 754−759. (23) Komolov, A. S.; Lazneva, E. F.; Pshenichnyuk, S. A.; Chepilko, N. S.; Tomilov, A. A.; Gerasimova, N. B.; Lezov, A. A.; Repin, P. S. Electronic Properties of the Interface Between Hexadecafluoro Copper Phthalocyanine and Unsubstituted Copper Phthalocyanine Films. Semiconductors 2013, 47 (7), 956−961. (24) Scheer, A. M.; Burrow, P. D. π* Orbital System of Alternating Phenyl and Ethynyl Groups: Measurements and Calculations. J. Phys. Chem. B 2006, 110, 17751−17756. (25) Tomasi, J.; Persico, M. Molecular Interactions in Solution: An Overview of Methods Based on Continuous Distributions of the Solvent. Chem. Rev. 1994, 94, 2027−2094. (26) Betowski, L. D.; Enlow, M.; Riddick, L.; Aue, D. H. Calculation of Electron Affinities of Polycyclic Aromatic Hydrocarbons and Solvation Energies of Their Radical Anion. J. Phys. Chem. A 2006, 110, 12927−12946.
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We acknowledge Saint-Petersburg State University (research grant 11.38.219.2014) and the Russian Foundation for Basic Research (grant nos. 14-03-00087 and 15-02-02809). We are grateful to the reviewers for useful comments and suggestions.
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DOI: 10.1021/acs.jpclett.5b00368 J. Phys. Chem. Lett. 2015, 6, 1104−1110
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DOI: 10.1021/acs.jpclett.5b00368 J. Phys. Chem. Lett. 2015, 6, 1104−1110
