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Oct 6, 2015 - ABSTRACT: Melanin is the pigment found in human skin that is responsible for both photoprotection and photodamage. Recently there have ...
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Feasibility of Ionization-Mediated Pathway for Ultraviolet-Induced Melanin Damage Mukunda Mandal, Tamal Das, Baljinder K. Grewal, and Debashree Ghosh* Physical and Materials Chemistry Division, CSIR-National Chemical Laboratory, Pune 411008, India S Supporting Information *

ABSTRACT: Melanin is the pigment found in human skin that is responsible for both photoprotection and photodamage. Recently there have been reports that greater photodamage of DNA occurs when cells containing melanin are irradiated with ultraviolet (UV) radiation, thus suggesting that the photoproducts of melanin cause DNA damage. Photoionization processes have also been implicated in the photodegradation of melanin. However, not much is known about the oxidation potential of melanin and its monomers. In this work we calculate the ionization energies of monomers, dimers, and few oligomers of eumelanin to estimate the threshold energy required for the ionization of eumelanin. We find that this threshold is within the UV-B region for eumelanin. We also look at the charge and spin distributions of the various ionized states of the monomers that are formed to understand which of the ionization channels might favor monomerization from a covalent dimer.

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the mechanism of decay following photoexcitation.8,15,24,29−34 Excited-state proton transfer, radical-cationic intermediates, and out-of-plane bending modes have been proposed to explain the nonradiative decay.7,8,31,35−37 Apart from its monotonic absorption spectra, eumelanin is important in processes involving oxidative damage, such as quenching of reactive oxygen species and binding to metals. Recently there has been some interest in the electron-transfer processes in melanin and its use as a solar cell material.7,13,28,38 Thus, its oxidation potential is a property of considerable interest. Radical cations have been proposed as intermediates that are involved in the deactivation of melanin monomer following photoexcitation. Local oxidation potential is also important in the understanding of aging processes in skin. However, very little quantitative data exist about the oxidation potential of the various melanin forms.38−40 A recent study41 shows that UV-A- and UV-B-induced processes in melanin proceed via different mechanisms. They also show that eumelanin and pheomelanin react differently toward UV radiation. It has been proposed that UV exposure causes excitation and photoionization processes, both of which are important in carcinogenic properties of melanin. They argue that these processes cause degradation of melanin into fragments and might allow the fragmented moieties to closely approach DNA, thus causing DNA damage.

INTRODUCTION The pigment melanin is quite ubiquitous in nature and occurs in a broad range of colors.1,2 For humans, it originates in the epidermal melanocyte and protects us from a broad range of radiations.3 Melanin has many variants (eumelanin, pheomelanin, neuromelanin, etc.), and among them eumelanin is the most widely studied variant, since it has been known for its photoprotective properties against ultraviolet (UV) radiation. It is known to prevent oxidative damage and has been implicated in Alzheimer’s disease.4−8 There have been suggestions that melanin-inspired biomimetic materials can be used for applications such as bioelectronics, chemical sensing, and photon detection.9−11 However, quite paradoxically, it is also implicated in phototoxicity and carcinogenesis.12,13 For such an important pigment, very little is definitively known about the mechanism of its various photoprocesses.10,14,15 One of the major impediments in understanding melanin-related processes is the difficulty in understanding the structure of melanin due to its extreme heterogeneity and inability to crystallize.16 It is also highly insoluble in common solvents, giving rise to difficulties in experimental characterization.17 Most of the research on eumelanin has been focused toward understanding the origin of the broadband excitation spectrum and its monotonic frequency dependence.18−25 Initially, the broadband spectra of melanin was explained by an organic semiconductor model and ascribed to the band structure.26,27 However, recent studies strongly point toward heterogeneity to be the primary cause behind this.8,28 Spectroscopic measurements and computational studies have been used to understand © 2015 American Chemical Society

Received: September 8, 2015 Revised: October 6, 2015 Published: October 6, 2015 13288

DOI: 10.1021/acs.jpcb.5b08750 J. Phys. Chem. B 2015, 119, 13288−13293

Article

The Journal of Physical Chemistry B

calculations were performed with the quantum chemistry package Q-Chem.50 The stacked homo- and heterodimers in the ground state were optimized with the RIMP2/6-311++G(d,p) level of theory. To understand the interactions of homo dimerization, we have computed constrained optimized geometries (constrained in the symmetry, both parallel and antiparallel), as well as the slightly displaced geometries to understand the effect of slip stacking (given in Table S6). Finally, we have also optimized (with the RIMP2/6-31+G(d,p) level of theory) the completely relaxed geometry of the homodimers that are capped with methyl groups to prevent H-bonding. To elucidate the effect of methylation in the monomers, their ionization energies were calculated and are reported in Table S3. The Hbonded homo- and heterodimers were also optimized with RIMP2/6-31+G(d,p) and constrained to be in-plane. For the stacked and H-bonded dimers, we have computed the VIEs with EOM-IP-CCSD/6-31+G(d,p) and ωB97x-D/6311++G(d,p) levels of theory.

The goal of this work is to provide high-level benchmark calculations of ionization energies (IEs) of monomers of eumelanin and their oligomers. The results are used to ascertain the feasibility of ionization-mediated processes that are induced by UV radiation on melanin. We also examine the spin densities and charge distributions of the lowest few ionized states, to understand the preferential charge generation on the various C atoms. Chart 1 shows the monomers of eumelanin that are considered in this study. Eumelanin is mainly made up of Chart 1. Monomers of Eumelanin at Different Oxidation States

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dihydroxyindole (DHI) and carboxylated dihydroxyindole (DHICA). Various oxidation and tautomeric states of these species such as the indole quinone (IQ) and semiquinone (SQ) are also present in melanin.28 Here, we refer to semiquinone and indolequinone tautomers as MKI and DKI, respectively. Because carboxylation has less effect on the spectra and the oxidation potential, we do not consider DHICA separately.

RESULTS AND DISCUSSION Monomers. Table 1 shows the comparison between the lowest VIEs, Koopmans’ IEs, and AIEs of the monomers DHI,

Table 1. VIEs, AIEs, and the Koopmans’ IEs (eV) for the Monomers at the EOM-IP-CCSD/6-311++G(d,p) Level of Theorya

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COMPUTATIONAL DETAILS Our method of choice for the vertical and adiabatic ionization energies (VIEs and AIEs) is equation of motion ionization potential coupled cluster with single and double excitations (EOM-IP-CCSD).42−48 EOM-IP-CCSD is spin-contaminationfree and does not suffer from unphysical symmetry breaking. The CCSD method is used to characterize the neutral closed shell state, while Koopmans-like excitation operator (R̂ ) is applied to target the complicated open shell ionized states Ψgs = exp(T̂ )Ψ0 (1) Ψis = R̂ exp(T̂ )Ψ0

(2)

† R̂ = R1̂ + R̂ 2 = ra i î + rijkaî aĵ ak̂

(3)

species

VIE

AIE

Koopmans’ energy

DHI MKI DKI

7.31 (0.9642) 8.53 (0.9616) 7.98 (0.9618)

7.00 8.16 7.79

7.40 8.71 8.27

a The parentheses contain the |R1| amplitude of the most significant transition.

MKI, and DKI. We notice that the AIEs (signifying the onset of ionization process) are lower than the VIEs by about 0.2−0.4 eV. This is important to note because for the largest oligomers we have calculated only the VIEs; thus, it is safe to assume that the onset of ionization is lower by at least 0.2−0.4 eV from the calculated VIEs. We also notice that all the ionizations are well characterized by Koopmans’ theorem (error from EOM-IP calculated VIE ≤ 0.3 eV). The Koopmans-like nature of the ionizations is also seen from the large (greater than 0.9) R1 amplitudes (values in parentheses in Table 1). The single, large R1 amplitude ionization, signifying predominant removal of electron from a single Hartree−Fock (HF) MO, is seen in the case of all the lowest five ionized states of DHI and DKI (Figure 1 and Table S2). However, in the case of MKI, the higher ionized states (second ionized state onward) show significant deviation from Koopmans-like states because the electron removal happens from more than one HF MO. The nature of the lowest few ionized states of DHI is in good agreement with the experimental results obtained for related compounds such as indole and 5-hydroxy indole.51 The effect of using different methods and basis sets for these calculations are shown in detail in Table S1. Benchmarking against the rigorous EOM-IP-CCSD/cc-pVTZ level of theory, errors in the ωB97x-D method with different basis sets were found to be around 0.1 eV for all the monomers. Thus, for estimating the threshold ionizations of the largest oligomers we have used the more computationally affordable ωB97x-D/631+G(d,p) and ωB97x-D/6-311++G(d,p) levels of theory.

where R̂ consists of 1-hole and 2-hole−1-particle operators. Ψgs and Ψis are the wave functions of the ground and ionized states, respectively. We also use EOM-IP-CCSD to calculate the charge and spin distributions of the various ionized states. Density functional theory with ωB97x-D functional (long-range and dispersion-corrected)49 is used to calculate the lowest ionization energies of the larger oligomers. We have considered the three oxidation states (Chart 1) of the eumelanin monomers. The monomers in their ground state were optimized with the RIMP2/cc-pVTZ level of theory. The geometries are reported in the Supporting Information. Because unrestricted MP2 is known to suffer from spincontamination and overestimation of charge localization, RIMP2 is not the method of choice for the cation geometry optimization. The cations of the monomers were optimized with the ωB97x-D/cc-pVTZ level of theory. The VIEs of monomers were calculated with EOM-IP-CCSD and ωB97x-D methods with cc-pVTZ, 6-311++G(d,p) and 6-31+G(d,p) basis sets. The adiabatic ionization energies (AIEs) were also calculated with EOM-IP-CCSD and ωB97x-D methods. All 13289

DOI: 10.1021/acs.jpcb.5b08750 J. Phys. Chem. B 2015, 119, 13288−13293

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Figure 2. HF MOs for the leading R1 amplitudes plotted for the (a) DHI-DKI and (b) DHI-MKI stacked dimers. 61.6% and 96.2% of the spin are localized on the DHI in DHI-DKI and DHI-MKI dimers, respectively.

Figure 1. Lowest five VIEs (at the EOM-IP-CCSD/6-31+G(d,p) level of theory) of the monomers DHI, MKI, and DKI. Hartree−Fock MOs corresponding to the significant R1 amplitudes are plotted to show the nature of the ionized states, i.e., π or σ type MOs and whether the ionization predominantly happens from one or more MOs.

DHI monomer has the lowest VIE, and DHI-DHI stacking causes the maximum reduction in VIE. Therefore, to estimate the asymptotic effect of multiple stacks of monomers, we focus on the DHI-DHI stacks. Parallel and antiparallel stacks of trimers, tetramers, etc. with DHI are considered (without optimization). The change in VIEs (ΔVIEs) for these oligomers with respect to monomer are shown in Figure 3a. We see that the cumulative effect of stacks of DHI is approximately −1.44 eV in parallel (bringing the asymptotic value of VIE to 5.79 eV) and −1.19 eV (asymptotic value of VIE at 6.04 eV) in antiparallel orientations (by exponential fitting to y = a + be−cx). The MKI-MKI and DKI-DKI stacks have asymptotic VIEs in the range of 7.46−8.35 eV and 7.14−7.26 eV, respectively (given in Figure S2). With increase in the number of stacked oligomers, we also notice a spin or charge localization on the monomers situated in the middle (given in Figure 3b). In stacked DHI oligomers, because the spin/charge is localized on a few monomers, this would give rise to preferential melanin damage pathways. The localized charges on the monomers can cause large changes in the partial charges on the C atoms. Therefore, a C−C bond formed between an ionized monomer and its neighboring one (in the melanin oligomeric structure) would be polar in nature and thus would be more easily damaged. Table 3 shows the effect of H-bonding interactions on the ionization energies. It is important to note that because the VIE of DHI is significantly lower than MKI and DKI, ΔVIE for all heterodimers containing DHI have been calculated as the difference from DHI monomer. For DKI-MKI species, the ΔVIE is calculated from DKI. All H-bonded structures are optimized in planar geometry, i.e., Cs symmetry. The DHI-DHI and DHI-MKI ΔVIEs are small because of opposing effects of H-bond donation and acceptance by the phenolic OH of the DHI. On the other hand, DKI is only a H-bond acceptor and therefore causes maximum change in VIE (DHI-DKI dimer). Figure 4 shows the most important MOs involved in the lowest few ionized states of various H-bonded dimers and trimers. The positive charge (hole) formed in the ionized states is localized on one monomer. The lowest ionization is always from the highest occupied molecular orbital of the DHI moiety. This is surprisingly valid even for DHI dimer because one DHI molecule is the H-bond donor (causes lowering in VIE). Among the dimers, the maximum shift in VIE is noticed in the case of DHI-DKI dimers. Because DKI is the best H-bond acceptor (two keto groups), the VIE of DHI is reduced most in DHI-DKI dimer (−0.79 and −0.44 eV). A trimer with 2 Hbonded DKI with DHI would be expected to show the maximum total effect of H-bonding on the VIE of DHI. The ΔVIE in DKI-DHI-DKI trimer is approximately −1.6 eV.

Effect of Stacking and H-Bonding. The effect of stacking interactions of the dimers on VIE is quantified by considering various constrained optimized structures. The stacked structures of the homodimers are formed by restricting the 2 monomers in Cs and Ci symmetries for parallel and antiparallel geometries, respectively. This approach is taken to evaluate only the effect of stacking (and avoid H-bonding interactions). From Table 2, we notice that the VIEs are reduced by 0.7− 0.8 eV for DHI-DHI, 0.22−0.47 eV for MKI-MKI, and 0.39− Table 2. VIEs of the Stacked Hetero- and Homodimers of DHI, MKI, and DKI (EOM-IP-CCSD/6-31+G(d,p) Level of Theory)a species DHI-DHI DHI-MKI DHI-DKI MKI-MKI DKI-DKI DKI-MKI

parallel 6.43 7.46 7.17 7.99 7.39 7.78

(−0.80) (+0.23) (−0.06) (−0.47) (−0.52) (−0.13)

antiparallel 6.53 (−0.70) 7.56 (+0.33) 7.26 (+0.03) 8.24 (−0.22) 7.52 (−0.39) n.a.b

a The change in VIEs with respect to the monomers (ΔVIEs) are given in parentheses. bThe DKI-MKI stacked antiparallel structure is not a stable minima.

0.52 eV for DKI-DKI dimers. The parallel conformation of the homodimers causes more change in VIE than the antiparallel conformation because of more orbital overlap and delocalization. In all the homodimers other than MKI-MKI and DKI-DKI antiparallel structures, stacking interaction preferentially stabilizes the cationic species over the neutral species; thus, there is a significant lowering of VIE of the dimer. However, this kind of lowering is not as much in the case of antiparallel conformations of keto containing MKI-MKI and DKI-DKI species, which can be ascribed to the large dipole−dipole stabilization interaction in the neutral species. Because in MKIMKI and DKI-DKI antiparallel conformation, both neutral and cationic species are stabilized by dimerization, there is very little overall effect on VIE. In the case of homodimers, the total positive charge (hole) is delocalized on both the monomers (given in Figure S1). For the stacked heterodimer cations, the positive charge is localized preferentially on the DHI moiety (Figure 2). The change in VIEs due to heterodimer stacking is lower because of less delocalization of the positive charge. 13290

DOI: 10.1021/acs.jpcb.5b08750 J. Phys. Chem. B 2015, 119, 13288−13293

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Figure 3. Effect of stacking on the ionized states of DHI.

Table 3. VIEs of the H-Bonded Hetero- and Homodimers of DHI, MKI, and DKI (EOM-IP-CCSD/6-31+G(d,p) Level of Theory)a species

OH

DHI-DHI DHI-DKI DHI-MKI DKI-DKI MKI-DKI MKI-MKI

7.12 (−0.11) 6.44 (−0.79) 7.37 (+0.14) n.a.b 7.76 (−0.70) 8.31 (−0.15)

NH n.a. 6.79 6.91 6.89 7.43 n.a.c

(−0.44) (−0.32) (−1.02) (−0.48)

a

The change in VIEs with respect to the monomers (ΔVIEs) are given in parentheses. The OH and NH labels are used to denote the H-bond donor site. bDKI does not have phenolic OH; therefore, there are no possible DKI-DKI OH structures. cMKI-MKI NH structure is not a stable minima.

Figure 5. VIEs of monomers, dimers, and oligomers of DHI. The lowest few VIEs of the monomer and dimers are calculated with EOMIP-CCSD/6-31+G(d,p). For the oligomers, only the lowest VIEs are marked at the ωB97x-D/6-311++G(d,p) level of theory.

Distribution of Positive Charge. To investigate feasible pathways for UV-mediated melanin damage, we probe the charge and spin densities of the monomers in their lowest ionized states. Figure 6 shows the difference in natural bond orbital charges of the lowest ionized states from the ground state (neutral) calculated at the EOM-IP-CCSD/6-31+G(d,p) level of theory. We concentrate on the C atoms that are available for dimerization (C2, C3, C4, and C7). We notice that in the first ionized state C2 has a significant positive charge on it. In the second ionized state, the positive charge is localized on the C3, C4, and C7 atoms. Thus, the C−C bonds (between covalent dimers) from C2, C3, C4, and C7 will be significantly polar after ionization. Therefore, these ionized states can be effective channels for melanin damage and monomerization (i.e., C−C bond breaking in covalent dimers).

The effect of stacking and H-bonding interactions on VIEs is a combination of extent of orbital overlap, delocalization, and electrostatic perturbations due to the environment. In the case of stacking interactions, orbital overlap and delocalization have been found to be the most important factors.52 On the other hand, electrostatic (Coloumbic and polarization) interactions are mainly important in the case of H-bonds; thus, the change in IE from H-bonds is also electrostatic in origin. Figure 5 shows the lowest few VIEs of the monomers compared to the stacked and H-bonded dimers as well as stacked oligomers. We see the reduction in VIEs due to oligomerization. Because the asymptotic effect of stacking in DHI is around −1.4 eV and the effect of H-bonding is −1.6 eV, the overall reduction in VIE is approximately 3.0 eV. The threshold of IE can be estimated to be 4.23 eV, which is in good agreement with the experimental threshold of 4.6 ± 0.2 eV.38 Because the experimental VIE is for melanosome, which has substantial contribution from proteins and metals, a better comparison might be with experiments on thin films of melanin.53

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CONCLUSION In summary, we have calculated the effect of H-bonding and stacking on the ionization energies of the eumelanin monomers (DHI, MKI, and DKI). DHI has the lowest VIE among these

Figure 4. Hartree−Fock MOs corresponding to the most significant R1 amplitudes for the three lowest ionized states of the H-bonded DHI oligomers. 13291

DOI: 10.1021/acs.jpcb.5b08750 J. Phys. Chem. B 2015, 119, 13288−13293

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Figure 6. Change in the charge distribution due to different ionized states in DHI monomer.

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ACKNOWLEDGMENTS We thank CSIR for the XIIth five year plan on Multiscale modelling and DST for funding. B.K.G. thanks CSIR for Nehru postdoctoral fellowship.

species and therefore is of particular interest to us. In general, both H-bonding and stacking causes lowering of the IEs of DHI. The effect of stacking interactions on the VIE is due to orbital overlap and stabilization of the cation by delocalization of charge. H-bond donation causes decrease in IE, and H-bond acceptance causes increase in IE. However, in DHI it is almost always a balance between H-bond donation and acceptance that in general decreases its VIE. Because DKI is the most effective H-bond acceptor, the DKI-DHI H-bonded complex causes the maximum decrease in VIE. It is also noticed that the overall effect of H-bond on the VIE is much more pronounced than the effect of stacking. The threshold of VIE is found to be 4.2− 4.3 eV. The AIE of the monomers are lower than the VIEs by 0.2−0.4 eV. Thus, the possible ionizations in melanin can start from around 4.0 eV, which is in the UV-B region of radiation (3.9−4.4 eV). Subsequent to ionization, the positive charge is preferentially localized on the one or few DHI moiety. We have also calculated the NBO charge distribution (hole delocalization) on the DHI monomer for its lowest ionized states to understand which ionized state might be responsible for a reactive carbon species and thereby melanin damage and fragmentation. To the best of our knowledge, this is the first work that computationally estimates the ionization energies for the possible dimers and oligomers in melanin and the threshold energy from which ionization is possible in melanin. It also shows that this threshold energy is in the UV-B region; therefore, UV-B-mediated melanin damage can indeed occur via an ionized intermediate. Work is in progress to understand the melanin damage pathway after ionization.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.5b08750. Effect of basis and methods, details of R1 amplitudes of ionizations, ionization energies (AIE and VIE) of various dimers, molecular orbital pictures, details of the exponential fit for asymptotic values, and all the Cartesian coordinates of the species used in this study (PDF)

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REFERENCES

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: +91 20 2590 3052. Notes

The authors declare no competing financial interest. 13292

DOI: 10.1021/acs.jpcb.5b08750 J. Phys. Chem. B 2015, 119, 13288−13293

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DOI: 10.1021/acs.jpcb.5b08750 J. Phys. Chem. B 2015, 119, 13288−13293