Tetramethylalloxazines as efficient singlet oxygen photosensitizers and potential redox-sensitive agents
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
2017/27/B/ST4/02494 (OPUS)
The National Science Centre of Poland (NCN)
2017/27/B/ST4/02494 (OPUS)
The National Science Centre of Poland (NCN)
2013/08/T/ST4/00640 (Etiuda)
The National Science Centre of Poland (NCN)
CEUS-UNISONO 2020/02/Y/ST4/00042
The National Science Centre of Poland (NCN)
CEUS-UNISONO 2020/02/Y/ST4/00042
The National Science Centre of Poland (NCN)
2017/27/B/ST4/02494 (OPUS)
The National Science Centre of Poland (NCN)
CEUS-UNISONO 2020/02/Y/ST4/00042
The National Science Centre of Poland (NCN)
2017/27/B/ST4/02494 (OPUS)
The National Science Centre of Poland (NCN)
2017/27/B/ST4/02494 (OPUS)
The National Science Centre of Poland (NCN)
no. POIR.04.02.00-00-C004/19-00
the Polish Roadmap Project NEBI
no. POIR.04.02.00-00-C004/19-00
the Polish Roadmap Project NEBI
no. POIR.04.02.00-00-C004/19-00
the Polish Roadmap Project NEBI
Grant No. US/2021/31/SC
Polish-U.S. Fulbright Commission
21-14200K
the Czech Science Foundation
Homing grant no POIR.04.04.00-00-441F/17-00
the Foundation for Polish Science (FNP)
PubMed
37591918
PubMed Central
PMC10435492
DOI
10.1038/s41598-023-40536-4
PII: 10.1038/s41598-023-40536-4
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
Tetramethylalloxazines (TMeAll) have been found to have a high quantum yield of singlet oxygen generation when used as photosensitizers. Their electronic structure and transition energies (S0 → Si, S0 → Ti, T1 → Ti) were calculated using DFT and TD-DFT methods and compared to experimental absorption spectra. Generally, TMeAll display an energy diagram similar to other derivatives belonging to the alloxazine class of compounds, namely π,π* transitions are accompanied by closely located n,π* transitions. Photophysical data such as quantum yields of fluorescence, fluorescence lifetimes, and nonradiative rate constants were also studied in methanol (MeOH), acetonitrile (ACN), and 1,2-dichloroethane (DCE). The transient absorption spectra were also analyzed. To assess cytotoxicity of new compounds, a hemolytic assay was performed using human red blood cells (RBC) in vitro. Subsequently, fluorescence lifetime imaging experiments (FLIM) were performed on RBC under physiological and oxidative stress conditions alone or in the presence of TMeAll allowing for pinpointing changes caused by those compounds on the intracellular environment of these cells.
Department of Chemistry Allegheny College 520 N Main Street Meadville PA USA
Faculty of Biology Adam Mickiewicz University Uniwersytetu Poznańskiego 6 61 614 Poznan Poland
Faculty of Chemistry Adam Mickiewicz University Uniwersytetu Poznańskiego 8 61 614 Poznan Poland
Faculty of Physics Adam Mickiewicz University Uniwersytetu Poznańskiego 2 61 614 Poznan Poland
Institute of Bioorganic Chemistry Polish Academy of Sciences Noskowskiego 12 14 61 704 Poznan Poland
Poznań University of Economics and Business Al Niepodległości 10 61 875 Poznan Poland
Zobrazit více v PubMed
Rajendar B, Nishizawa S, Teramae N. Alloxazine as a ligand for selective binding to adenine opposite AP sites in DNA duplexes and analysis of single-nucleotide polymorphisms. Org. Biomol. Chem. 2008;6:670–673. doi: 10.1039/b719786a. PubMed DOI
Wang ZW, Rizzo CJ. Regioselective synthesis of β-N1-and β-N3-alloxazine nucleosides. Org. Lett. 2000;2:227–230. doi: 10.1021/ol9913338. PubMed DOI
Dalton SR, et al. DNA binding by Ru(II)-bis(bipyridine)-pteridinyl complexes. J. Biol. Inorg. Chem. 2008;13:1133–1148. doi: 10.1007/s00775-008-0399-y. PubMed DOI
Miyazaki S, Kojima T, Fukuzumi S. Photochemical and thermal isomerization of a ruthenium(II)-alloxazine complex involving an unusual coordination mode. J. Am. Chem. Soc. 2008;130:1556–1557. doi: 10.1021/ja077954a. PubMed DOI
Valerón Bergh VJ, Bruzell E, Hegge AB, Tønnesen HH. Influence of formulation on photoinactivation of bacteria by lumichrome. Pharmazie. 2015;70:574–580. doi: 10.1691/ph.2015.5006. PubMed DOI
Grininger M, Zeth K, Oesterhelt D. Dodecins: A family of lumichrome binding proteins. J. Mol. Biol. 2006;357:842–857. doi: 10.1016/j.jmb.2005.12.072. PubMed DOI
Grininger M, Staudt H, Johansson P, Wachtveitl J, Oesterhelt D. Dodecin is the key player in flavin homeostasis of archaea. J. Biol. Chem. 2009;284:13068–13076. doi: 10.1074/jbc.M808063200. PubMed DOI PMC
Tsukamoto, S., Kato, H., Hirota, H. & Fusetani, N. Lumichrome is a putative intrinsic substance inducing larval metamorphosis in the ascidian Halocynthia roretzi. Biol. Ascidians, 335–340 (2001).
Tsukamoto S, Kato H, Hirota H, Fusetani N. Lumichrome - A larval metamorphosis-inducing substance in the ascidian Halocynthia roretzi. Eur. J. Biochem. 1999;264:785–789. doi: 10.1046/j.1432-1327.1999.00642.x. PubMed DOI
Reddy HL, et al. Toxicity testing of a novel riboflavin-based technology for pathogen reduction and white blood cell inactivation. Transf. Med. Rev. 2008;22:133–153. doi: 10.1016/j.tmrv.2007.12.003. PubMed DOI
Miskolczy Z, Biczok L. Anion-induced changes in the absorption and fluorescence properties of lumichrome: A new off-the-shelf fluorescent probe. Chem. Phys. Lett. 2005;411:238–242. doi: 10.1016/j.cplett.2005.06.049. DOI
Sikorska E, Sikorski M, Steer RP, Wilkinson F, Worrall DR. Efficiency of singlet oxygen generation by alloxazines and isoalloxazines. J. Chem. Soc. Faraday Trans. 1998;94:2347–2353. doi: 10.1039/a802340i. DOI
Sikorski M, et al. Photophysical properties of lumichromes in water. J. Photochem. Photobiol. B. 2001;60:114–119. doi: 10.1016/S1011-1344(01)00134-8. PubMed DOI
Sikorski M, Sikorska E, Moreno RG, Bourdelande JL, Worrall DR. Photophysics of methyl substituted alloxazines in water: Efficiency of singlet oxygen generation. J. Photochem. Photobiol. A. 2002;149:39–44. doi: 10.1016/S1010-6030(01)00651-7. DOI
Tatsumi K, Ichikawa H, Wada S. Flavin-sensitized photooxidation of substituted phenols in natural-water. J. Contam. Hydrol. 1992;9:207–219. doi: 10.1016/0169-7722(92)90059-N. DOI
Sikorska E, Koziołowa A. Excited state proton transfer of methyl- and cyano-substituted alloxazines in the presence of acetic acid. J. Photochem. Photobiol. A. 1996;95:215–221. doi: 10.1016/1010-6030(95)04258-X. DOI
Kasha M. Proton-transfer spectroscopy - perturbation of the tautomerization potential. J. Chem. Soc. Faraday Trans. 1986;82:2379–2392. doi: 10.1039/f29868202379. DOI
Song PS, Sun M, Koziołowa A, Kozioł J. Photoautomerism of lumichromes and alloxazines. J. Am. Chem. Soc. 1974;96:4319–4323. doi: 10.1021/ja00820a045. DOI
Koziołowa A. Solvent and methyl substituent effect on phototautomerism and ionization of alloxazines. Photochem. Photobiol. 1979;29:459–471. doi: 10.1111/j.1751-1097.1979.tb07076.x. DOI
Sikorska E, et al. In search of excited-state proton transfer in the lumichrome dimer in the solid state: Theoretical and experimental approach. J. Phys. Chem. A. 2006;110:4638–4648. doi: 10.1021/jp060072y. PubMed DOI
Sikorska E, et al. Ground- and excited-state double proton transfer in lumichrome/acetic acid system: Theoretical and experimental approach. J. Phys. Chem. A. 2005;109:11707–11714. doi: 10.1021/jp053951d. PubMed DOI
Zen YH, Wang CM. A novel optical transistor device based on photoinduced proton-transfer reactions. J. Chem. Soc. Chem. Commun. 1994 doi: 10.1039/C39940002625. DOI
Sikorska E, et al. Spectroscopy and photophysics of mono methyl-substituted alloxazines. Chem. Phys. 2004;301:95–103. doi: 10.1016/j.chemphys.2004.03.005. DOI
Sikorska E, Khmelinskii IV, Worrall DR, Koput J, Sikorski M. Spectroscopy and photophysics of iso- and alloxazines: Experimental and theoretical study. J. Fluoresc. 2004;14:57–64. doi: 10.1023/B:JOFL.0000014660.59105.31. PubMed DOI
Insińska-Rak M, Golczak A, Sikorski M. Photochemistry of riboflavin derivatives in methanolic solutions. J. Phys. Chem. A. 2012;116:1199–1207. doi: 10.1021/jp2094593. PubMed DOI
Sikorski M, et al. Spectroscopy and photophysics of dimethyl-substituted alloxazines. J. Photochem. Photobiol. A. 2008;200:148–160. doi: 10.1016/j.jphotochem.2008.07.006. DOI
Bruszyńska M, et al. Electronic structure and spectral properties of selected trimethyl-alloxazines: Combined experimental and DFT study. Chem. Phys. 2009;361:83–93. doi: 10.1016/j.chemphys.2009.05.011. DOI
Kar RK, Miller AF, Mroginski MA. Understanding flavin electronic structure and spectra. Wiley Interdiscip. Rev. Comput. Mol. Sci. 2021 doi: 10.1002/wcms.1541. DOI
Kar RK, Chasen S, Mroginski MA, Miller AF. Tuning the quantum chemical properties of flavins via modification at C8. J. Phys. Chem. B. 2021;125:12654–12669. doi: 10.1021/acs.jpcb.1c07306. PubMed DOI
Cibulka, R. & Fraaije, M. Flavin-Based Catalysis (Wiley‐VCH, 2021) 10.1002/9783527830138,2021.
Tolba AH, Vávra F, Chudoba J, Cibulka R. Tuning flavin-based photocatalytic systems for application in the mild chemoselective aerobic oxidation of benzylic substrates. Eur. J. Org. Chem. 2020;1579–1585:2020. doi: 10.1002/ejoc.201901628. DOI
Mojr V, et al. Tailoring flavins for visible light photocatalysis: organocatalytic 2+2 cycloadditions mediated by a flavin derivative and visible light. Chem. Commun. 2015;51:12036–12039. doi: 10.1039/c5cc01344e. PubMed DOI
Farag MR, Alagawany M. Erythrocytes as a biological model for screening of xenobiotics toxicity. Chem. Biol. Interact. 2018;279:73–83. doi: 10.1016/j.cbi.2017.11.007. PubMed DOI
Shrirao AB, et al. Autofluorescence of blood and its application in biomedical and clinical research. Biotechnol. Bioeng. 2021;118:4550–4576. doi: 10.1002/bit.27933. PubMed DOI
Sierakowska A, Jasiewicz B, Piosik L, Mrówczyńska L. New C8-substituted caffeine derivatives as promising antioxidants and cytoprotective agents in human erythrocytes. Sci. Rep. 2023;13:1785. doi: 10.1038/s41598-022-27205-8. PubMed DOI PMC
Insińska-Rak M, et al. 5-Deazaalloxazine as photosensitizer of singlet oxygen and potential redox-sensitive agent. Photochem. Photobiol. Sci. 2023;22:1655–1671. doi: 10.1007/s43630-023-00401-9. PubMed DOI
Golczak A, et al. Photophysical properties of alloxazine derivatives with extended aromaticity - Potential redox-sensitive fluorescent probe. Spectrochim. Acta Part A. 2022;272:120985. doi: 10.1016/j.saa.2022.120985. PubMed DOI
Csoregh I, Kierkegaard P, Kozioł J, Müller F. The molecular and crystal-structures of 9-methyl- and 1,3,8,9-tetramethylalloxazines. Acta Crystallogr. Sec. B Struct. Sci. 1987;41:383–390. doi: 10.3891/acta.chem.scand.41b-0383. DOI
Sikorska E, et al. Spectroscopy and photophysics of lumiflavins and lumichromes. J. Phys. Chem. A. 2004;108:1501–1508. doi: 10.1021/jp037048u. DOI
Augustyniak W, et al. Transient effect in fluorescence quenching of S2-xanthione by 3,3-diethylpentane in perfluoroalkane solvent - a steady-state and dynamic approach. Pol. J. Chem. 1993;67:1409–1423.
Pędziński T, Markiewicz A, Marciniak B. Photosensitized oxidation of methionine derivatives. Laser flash photolysis studies. Res. Chem. Intermed. 2009;35:497–506. doi: 10.1007/s11164-009-0046-4. DOI
Jiménez-Banzo A, Ragàs X, Kapusta P, Nonell S. Time-resolved methods in biophysics. 7. Photon counting vs. analog time-resolved singlet oxygen phosphorescence detection. Photochem. Photobiol. Sci. 2008;7:1003–1010. doi: 10.1039/b804333g. PubMed DOI
Martí C, Jürgens O, Cuenca O, Casals M, Nonell S. Aromatic ketones as standards for singlet molecular oxygen O2(1Δg) photosensitization. Time-resolved photoacoustic and near-IR emission studies. J. Photochem. Photobiol. A. 1996;97:11–18. doi: 10.1016/1010-6030(96)04321-3. DOI
Schmidt R, Tanielian C, Dunsbach R, Wolff C. Phenalenone, a universal reference compound for the determination of quantum yields of singlet oxygen O2(1Δg) sensitization. J. Photochem. Photobiol. A. 1994;79:11–17. doi: 10.1016/1010-6030(93)03746-4. DOI
Becke AD. Density-functional thermochemistry. 3. The role of exact exchange. J. Chem. Phys. 1993;98:5648–5652. doi: 10.1063/1.464913. DOI
Lee CT, Yang WT, Parr RG. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron-density. Phys. Rev. B. 1988;37:785–789. doi: 10.1103/PhysRevB.37.785. PubMed DOI
Ditchfie R, Hehre WJ, Pople JA. Self-consistent molecular-orbital methods. 9. Extended gaussian-type basis for molecular-orbital studies of organic molecules. J. Chem. Phys. 1971;54:724–728. doi: 10.1063/1.1674902. DOI
Bauernschmitt R, Ahlrichs R. Treatment of electronic excitations within the adiabatic approximation of time dependent density functional theory. Chem. Phys. Lett. 1996;256:454–464. doi: 10.1016/0009-2614(96)00440-x. DOI
Frisch, M. J. et al. Gaussian 03, Revision C.02 Wallingford, CT, citeulike-article-id:3013967, (2003).
Greco I, et al. Correlation between hemolytic activity, cytotoxicity and systemic in vivo toxicity of synthetic antimicrobial peptides. Sci. Rep. 2020 doi: 10.1038/s41598-020-69995-9. PubMed DOI PMC
Neiss C, Saalfrank P, Parac M, Grimme S. Quantum chemical calculation of excited states of flavin-related molecules. J. Phys. Chem. A. 2003;107:140–147. doi: 10.1021/jp021671h. DOI
Martin CB, et al. The photochemistry of riboflavin tetraacetate and nucleosides. A study using density functional theory, laser flash photolysis, fluorescence, UV-Vis, and time resolved infrared spectroscopy. J. Phys. Chem. B. 2002;106:10263–10271. doi: 10.1021/jp026051v. DOI
Martin CB, Tsao ML, Hadad CM, Platz MS. The reaction of triplet flavin with indole. A study of the cascade of reactive intermediates using density functional theory and time resolved infrared spectroscopy. J. Am. Chem. Soc. 2002;124:7226–7234. doi: 10.1021/ja0123711. PubMed DOI
Rodríguez-Otero J, Martínez-Núñez E, Peña-Gallego A, Vázquez SA. The role of aromaticity in the planarity of lumiflavin. J. Org. Chem. 2002;67:6347–6352. doi: 10.1021/jo011159c. PubMed DOI
Sikorska E, Khmelinskii IV, Koput J, Sikorski M. Electronic structure of lumiflavin and its analogues in their ground and excited states. J. Mol. Struct. Theochem. 2004;676:155–160. doi: 10.1016/j.theochem.2004.02.007. DOI
Neiss C, Saalfrank P. Ab initio quantum chemical investigation of the first steps of the photocycle of phototropin: A model study. Photochem. Photobiol. 2003;77:101–109. doi: 10.1562/0031-8655(2003)077<0101:aiqcio>2.0.co;2. PubMed DOI
Sun M, Moore TA, Song PS. Molecular luminescence studies of flavins. I. The excited states of flavins. J. Am. Chem. Soc. 1972;94:1730–1740. doi: 10.1021/ja00760a052. PubMed DOI
Platenkamp RJ, Palmer MH, Visser A. Ab initio molecular-orbital studies of closed shell flavins. Eur. Biophys. J. 1987;14:393–402. doi: 10.1007/BF00254862. DOI
Insińska-Rak M, et al. Spectroscopy and photophysics of flavin-related compounds: 3-benzyl-lumiflavin. Photochem. Photobiol. Sci. 2005;4:463–468. doi: 10.1039/b503898g. PubMed DOI
Eweg JK, Müller F, Bebelaar D, Vanvoorst JDW. Spectral properties of (iso)alloxazines in the vapor-phase. Photochem. Photobiol. 1980;31:435–443. doi: 10.1111/j.1751-1097.1980.tb03725.x. DOI
Eweg JK, Müller F, Vandam H, Terpstra A, Oskam A. He(I) and He(II) photoelectron-spectra of alloxazines and isoalloxazines. J. Am. Chem. Soc. 1980;102:51–61. doi: 10.1021/ja00521a010. DOI
Eweg JK, et al. Molecular luminescence of some isoalloxazines in apolar solvents at various temperatures. Photochem. Photobiol. 1979;30:463–471. doi: 10.1111/j.1751-1097.1979.tb07164.x. DOI
Lim EC. Proximity effect in molecular photophysics - dynamic consequences of pseudo-Jahn-Teller interaction. J. Phys. Chem. 1986;90:6770–6777. doi: 10.1021/j100284a012. DOI
Tyagi A, Penzkofer A. Absorption and emission spectroscopic characterization of lumichrome in aqueous solutions. Photochem. Photobiol. 2011;87:524–533. doi: 10.1111/j.1751-1097.2010.00836.x. PubMed DOI
Sinha S, Gharat PM, Pal H, Dutta Choudhury S. Lumichrome tautomerism in alcohol-water mixtures: Effect of carbon chain length and mole fraction of alcohols. J. Mol. Liq. 2020;314:113621. doi: 10.1016/j.molliq.2020.113621. DOI
Dutta Choudhury S, Pal H. Intriguing tautomerism of lumichrome in binary aqueous solvent mixtures: Implications for probing microenvironments. J. Phys. Chem. B. 2016;120:11970–11977. doi: 10.1021/acs.jpcb.6b08777. PubMed DOI
Mal M, Mandal D. Phototautomerism of alloxazine in acetic acid – water solvent systems. J. Mol. Liq. 2021 doi: 10.1016/j.molliq.2020.114928. DOI
Mal M, Mandal D. Solvent and pH-sensitive fluorescence response of alloxazine. J. Photochem. Photobiol. A. 2021;404:112888. doi: 10.1016/j.jphotochem.2020.112888. DOI
Fugate RD, Song PS. Lifetime study of phototautomerism of alloxazine and lumichromes. Photochem. Photobiol. 1976;24:479–481. doi: 10.1111/j.1751-1097.1976.tb06858.x. DOI
Wilkinson F, Helman WP, Ross AB. Quantum yields for the photosensitized formation of the lowest electronically excited singlet-state of molecular-oxygen in solution. J. Phys. Chem. Ref. Data. 1993;22:113–262. doi: 10.1063/1.555934. DOI
Sikorski M, et al. Photophysics of lumichrome on cellulose. J. Photochem. Photobiol. A. 2003;156:267–271. doi: 10.1016/s1010-6030(02)00427-6. DOI
Quaranta M, Murkovic M, Klimant I. A new method to measure oxygen solubility in organic solvents through optical oxygen sensing. Analyst. 2013;138:6243–6245. doi: 10.1039/c3an36782g. PubMed DOI
Murov, S. L., Carmichael, I. & Hug, G. L. Handbook of Photochemistry. Second Edition edn, (Taylor & Francis, 1993).
Kwiatek D, et al. Surface modification of luminescent Ln(III) fluoride core-shell nanoparticles with acetylsalicylic acid (aspirin): Synthesis, spectroscopic and in vitro hemocompatibility studies. ChemMedChem. 2020;15:1490–1496. doi: 10.1002/cmdc.202000269. PubMed DOI
Pretorius E, Olumuyiwa-Akeredolu O-OO, Mbotwe S, Bester J. Erythrocytes and their role as health indicator: Using structure in a patient-orientated precision medicine approach. Blood Rev. 2016;30:263–274. doi: 10.1016/j.blre.2016.01.001. PubMed DOI
Corbin F. Pathogen inactivation of blood components: Current status and introduction of an approach using riboflavin as a photosensitizer. Int. J. Hem. 2002;76:253–257. doi: 10.1007/BF03165125. PubMed DOI
Buniowska I, Wronski N, Insińska-Rak M, Sikorski M, Wolnicka-Glubisz A. Tetraacetyl riboflavin derivative mediates caspase 3/7 activation via MAPK in A431 cells upon blue light influence. Photochem. Photobiol. 2023 doi: 10.1111/php.13806. PubMed DOI
Akasov RA, et al. Photodynamic therapy of melanoma by blue-light photoactivation of flavin mononucleotide. Sci. Rep. 2019 doi: 10.1038/s41598-019-46115-w. PubMed DOI PMC
Wangsuwan S, Meephansan J. Comparative study of photodynamic therapy with riboflavin-tryptophan gel and 13% 5-aminolevulinic acid in the treatment of mild to moderate acne vulgaris. Clin. Cosmet. Investig. Dermatol. 2019;12:805–814. doi: 10.2147/ccid.s227737. PubMed DOI PMC
Dad'ová J, Svobodová E, Sikorski M, König B, Cibulka R. Photooxidation of sulfides to sulfoxides mediated by tetra-o-acetylriboflavin and visible light. ChemCatChem. 2012;4:620–623. doi: 10.1002/cctc.201100372. DOI
Neveselý T, Svobodová E, Chudoba J, Sikorski M, Cibulka R. Efficient metal-free aerobic photooxidation of sulfides to sulfoxides mediated by a vitamin B2 derivative and visible light. Adv. Synth. Catal. 2016;358:1654–1663. doi: 10.1002/adsc.201501123. DOI