Convergent Proton-Transfer Photocycles Violate Mirror-Image Symmetry in a Key Melanin Monomer

Olsen, Seth; Riesz, Jennifer; Mahadevan, I. B.; Coutts, Aaron J.; Bothma, Jacques P.; Powell, B. J.; McKenzie, Ross H.; Smith, Sean C.; Meredith, Paul

doi:10.1021/ja069280u

Cited by 51 publications

(71 citation statements)

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“…The pK a values for these groups are 4.25, 9.76, and 13.2, respectively. 24,25 Assuming that these values do not change significantly upon covalent bonding of DHICA monomers, it can be inferred that under moderately acidic conditions the hydroxyl groups are fully protonated, but the carboxylic acid groups could be partially deprotonated. To address the influence of the protonation state of the carboxylic acid group on excited state deactivation, we performed studies at both acidic and neutral conditions.…”

Section: ■ Resultsmentioning

confidence: 99%

Superior Photoprotective Motifs and Mechanisms in Eumelanins Uncovered

et al. 2014

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Human pigmentation is a complex phenomenon commonly believed to serve a photoprotective function through the generation and strategic localization of black insoluble eumelanin biopolymers in sun exposed areas of the body. Despite compelling biomedical relevance to skin cancer and melanoma, eumelanin photoprotection is still an enigma: What makes this pigment so efficient in dissipating the excess energy brought by harmful UV-light as heat? Why has Nature selected 5,6-dihydroxyindole-2-carboxylic acid (DHICA) as the major building block of the pigment instead of the decarboxylated derivative (DHI)? By using pico-and femtosecond fluorescence spectroscopy we demonstrate herein that the excited state deactivation in DHICA oligomers is 3 orders of magnitude faster compared to DHI oligomers. This drastic effect is attributed to their specific structural patterns enabling multiple pathways of intra-and interunit proton transfer. The discovery that DHICA-based scaffolds specifically confer uniquely robust photoprotective properties to natural eumelanins settles a fundamental gap in the biology of human pigmentation and opens the doorway to attractive advances and applications.

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Section: ■ Resultsmentioning

confidence: 99%

Superior Photoprotective Motifs and Mechanisms in Eumelanins Uncovered

et al. 2014

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“…Thus, calculations suggest that the overall nonradiative relaxation in eumelanin building blocks takes place within a time <50 fs through state mixing and proton transfer, in apparent agreement with the transient absorption data recorded by femtosecond pump−probe experiments. 30 Yet, despite these and other advances, current understanding of the UV dissipation mechanisms and especially the radiative pathways has remained limited. Herein, we report a new approach to elucidate eumelanin fluorescence properties and dynamics which capitalizes on the recent development of water-soluble 5,6-dihydroxyindole polymers novel efficient experimental tools.…”

Section: ■ Introductionmentioning

confidence: 99%

Bottom-Up Approach to Eumelanin Photoprotection: Emission Dynamics in Parallel Sets of Water-Soluble 5,6-Dihydroxyindole-Based Model Systems

et al. 2012

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The molecular mechanisms by which the black eumelanin biopolymers exert their photoprotective action on human skin and eyes are still poorly understood, owing to critical insolubility and structural heterogeneity issues hindering direct investigation of excitation and emission behavior. Recently, we set up strategies to obtain watersoluble 5,6-dihydroxyindole (DHI)-based polymers as useful models for disentangling intrinsic photophysical properties of eumelanin components from aggregation and scattering effects. Herein, we report the absorption properties and ultrafast emission dynamics of two separate sets of DHI-based monomer−dimer−polymer systems which were made water-soluble by means of poly(vinyl alcohol) or by galactosyl-thio substitution. Data showed that dimerization and polymerization of DHI result in long-lived excited states with profoundly altered properties relative to the monomer and that glycosylation of DHI imparts monomer-like behavior to oligomers and polymers, due to steric effects hindering planar conformations and efficient interunit electron communication. The potential of S-glycation as an effective tool to probe and control emission characteristics of eumelanin-like polymers is disclosed.

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“…6 This species was assigned to a complex between the excited DHICA − and a buffer species formed through a diffusion process. 6 On the other hand, calculations by Olsen et al 9 suggested that the 5-and 6-OH groups of DHICA should be involved in an ESIPT process or multistep excited-state proton transfer (ESPT) to the solvent. This discrepancy between experimental and theoretical results motivated us to further examine the role of the OH groups of the carboxylate anion of DHICA in proton transfer.…”

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confidence: 99%

“…The rate of proton transfer (4.0 × 10 8 s −1 ) is similar to that of other medium strength photoacids. 28,35,37 With the help of quantum chemistry calculations, Olsen et al 9 discussed ESPT between all three monoanions of DHICA (CT-1 (5-O − ), CT-2 (6-O − ), and CA (COO − )). CT-1 to CT-2 ESIPT was concluded to occur and possibly a multistep proton transfer from CA with the solvent to form the rearranged anion CT-2.…”

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confidence: 99%

Excited-State Proton-Transfer Processes of DHICA Resolved: From Sub-Picoseconds to Nanoseconds

Corani

Pezzella

Pascher

et al. 2013

J. Phys. Chem. Lett.

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Excited-state proton transfer has been hypothesized as a mechanism for UV energy dissipation in eumelanin skin pigments. By using time-resolved fluorescence spectroscopy, we show that the previously proposed, but unresolved, excited-state intramolecular proton transfer (ESIPT) of the eumelanin building block 5,6-dihydroxyindole-2-carboxylic acid (DHICA) occurs with a time constant of 300 fs in aqueous solution but completely stops in methanol. The previously disputed excited-state proton transfer involving the 5-or 6-OH groups of the DHICA anion is now found to occur from the 6-OH group to aqueous solvent with a rate constant of 4.0 × 10 8 s −1 .SECTION: Spectroscopy, Photochemistry, and Excited States T he 5,6-dihydroxyindole-2-carboxylic acid (DHICA), a key product of tyrosine metabolism in cutaneous melanocytes, plays important roles in skin homeostasis as a major precursor with 5,6-dihydroxyindole (DHI) of eumelanin biopolymers, the dark pigments of human skin, hair, and eyes, 1 as an antioxidant, 2 and as a central mediator in cell−cell communication. 3 Eumelanins contain various proportions of DHICA-derived units ranging from only a few % up to >50% depending on the phenotype and organism. While eumelanins appear to be complex biopolymers in which the various units concur to determine the macroscopic properties at several levels of structural organization, redox states, and disorder, a detailed understanding of the photophysical behavior of key building blocks is crucial if structure−property−function relationships are to be drawn. The peculiar absorption features of eumelanin 4,5 and its former monomer DHI and DHICA might play a role in protecting the skin against UV radiation, though the UV-induced reaction mechanisms are largely unknown. Recent time-resolved spectroscopy work on DHICA 6−8 revealed a rich, pH-dependent photochemistry in aqueous buffer solution. At a pH where the carboxyl group of the molecule is fully protonated (e.g., pH 2.5), a red-shifted fluorescence band (λ max ≈ 430 nm) with a relatively short lifetime of 240 ps was observed and attributed to a zwitterionic species formed as a result of rapid excited-state intramolecular proton transfer (ESIPT) from the COOH group toward the NH group. 6 However, the actual transfer time and decay of the original excited state of the fully protonated molecule could not be resolved with the temporal resolution of the employed streak camera technique. By using femtosecond fluorescence upconversion (FU), we can now directly resolve this reaction step and show that it indeed proceeds on the sup-picosecond time scale.The deprotonated carboxylate anion DHICA − was observed to have a long (∼1.6 ns) lifetime in neutral (pH 7) buffer solution representing decay to a new species with a red-shifted fluorescence spectrum (λ max ≈ 450 nm) and a 2.4 ns lifetime. 6 This species was assigned to a complex between the excited DHICA − and a buffer species formed through a diffusion process. 6 On the other hand, calculations by Olsen et al. 9 suggested that...

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Convergent Proton-Transfer Photocycles Violate Mirror-Image Symmetry in a Key Melanin Monomer

Cited by 51 publications

References 25 publications

Superior Photoprotective Motifs and Mechanisms in Eumelanins Uncovered

Superior Photoprotective Motifs and Mechanisms in Eumelanins Uncovered

Bottom-Up Approach to Eumelanin Photoprotection: Emission Dynamics in Parallel Sets of Water-Soluble 5,6-Dihydroxyindole-Based Model Systems

Excited-State Proton-Transfer Processes of DHICA Resolved: From Sub-Picoseconds to Nanoseconds

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