Formation and detection of oxidant-generated tryptophan dimers in peptides and proteins
Open accessAbstract
Free radicals are produced during physiological processes including metabolism and the immune response, as well as on exposure to multiple external stimuli. Many radicals react rapidly with proteins resulting in side-chain modification, backbone fragmentation, aggregation, and changes in structure and function. Due to its low oxidation potential, the indole ring of tryptophan (Trp) is a major target, with this resulting in the formation of indolyl radicals (Trp•). These undergo multiple reactions including ring opening and dimerization which can result in protein aggregation. The factors that govern Trp• dimerization, the rate constants for these reactions and the exact nature of the products are not fully elucidated. In this study, second-order rate constants were determined for Trp• dimerization in Trp-containing peptides to be 2-6 × 10 8 M-1 s-1 by pulse radiolysis. Peptide charge and molecular mass correlated negatively with these rate constants. Exposure of Trp-containing peptides to steady-state radiolysis in the presence of NaN 3 resulted in consumption of the parent peptide, and detection by LC-MS of up to 4 different isomeric Trp-Trp cross-links. Similar species were detected with other oxidants, including CO 3•- (from the HCO 3- -dependent peroxidase activity of bovine superoxide dismutase) and peroxynitrous acid (ONOOH) in the presence or absence of HCO 3-. Trp-Trp species were also isolated and detected after alkaline hydrolysis of the oxidized peptides and proteins. These studies demonstrate that Trp• formed on peptides and proteins undergo rapid recombination reactions to form Trp-Trp cross-linked species. These products may serve as markers of radical-mediated protein damage, and represent an additional pathway to protein aggregation in cellular dysfunction and disease.
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Electron delocalisation on the indole ring causes Trp• radicals to undergo rapid dimerization to Trp-Trp cross-linked species with different C-C and C-N cross-linkages.
“As a consequence of electron delocalisation on the indole ring, Trp• radicals undergo rapid dimerization reactions to give Trp-Trp cross-linked species that produce isomers with different cross-linkages, C-C cross-linked and C-C cross-linked species. C-N [142,143], Figure 55.”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [142]
Cites
Reactivity of HO2/O− 2 radicals in aqueous solution
Bielski, B. H. J., Cabelli, D. E., Arudi, R. L., & Ross, A. B. (1985) · Journal of Physical and Chemical Reference Data · doi:10.1063/1.555739 · Cited by 2,169 · see citing works
Singlet oxygen-mediated damage to proteins and its consequences
Davies, M. J. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00817-9 · Cited by 996 · see citing works
Self-citationProtein oxidation and peroxidation
Davies, M. J. (2016) · Biochemical Journal · doi:10.1042/bj20151227 · Cited by 952 · see citing works
Self-citationGeneration and propagation of radical reactions on proteins
Hawkins, C. L., & Davies, M. J. (2001) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(00)00252-8 · Cited by 753 · see citing works
Self-citationMammalian Heme Peroxidases: From Molecular Mechanisms to Health Implications
Davies, M. J., Hawkins, C. L., Pattison, D. I., & Rees, M. D. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1927 · Cited by 556 · see citing works
Self-citationHensley, K., Maidt, M. L., Yu, Z., Sang, H., Markesbery, W. R., & Floyd, R. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08126.1998 · Cited by 508 · see citing works
Quantification of protein modification by oxidants
Hawkins, C. L., Morgan, P. E., & Davies, M. J. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.01.007 · Cited by 486 · see citing works
Self-citationHeinecke, J. W., Li, W., Daehnke, H. L., & Goldstein, J. A. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53581-x · Cited by 485 · see citing works
Cross-Linking in Adhesive Quinoproteins: Studies with Model Decapeptides
Burzio, L. A., & Waite, J. H. (2000) · Biochemistry · doi:10.1021/bi0002434 · Cited by 485 · see citing works
Stable markers of oxidant damage to proteins and their application in the study of human disease
Davies, M. J., Fu, S., Wang, H., & Dean, R. T. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00206-3 · Cited by 461 · see citing works
Self-citationReactive species formed on proteins exposed to singlet oxygen
Davies, M. J. (2004) · Photochemical & Photobiological Sciences · doi:10.1039/b307576c · Cited by 399 · see citing works
Self-citationMcCall, A. S., Cummings, C. F., Bhave, G. B., Vanacore, R., Page, A. W., & Hudson, B. G. (2014) · Cell · doi:10.1016/j.cell.2014.05.009 · Cited by 361 · see citing works
Peroxidasin forms sulfilimine chemical bonds using hypohalous acids in tissue genesis
Bhave, G. B., Cummings, C. F., Vanacore, R., Kumagai-Cresse, C., Ero-Tolliver, I. A., Rafi, M., Kang, J.-S., Pedchenko, V. K., Fessler, L. I., Fessler, J. H., et al. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.1038 · Cited by 266 · see citing works
Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque
Fu, S., Davies, M. J., Stocker, R., & Dean, R. T. (1998) · Biochemical Journal · doi:10.1042/bj3330519 · Cited by 256 · see citing works
Self-citationGracanin, M., Hawkins, C. L., Pattison, D. I., & Davies, M. J. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.04.015 · Cited by 252 · see citing works
Self-citationFormation of disulfide bonds in proteins and peptides
Bulaj, G. W. (2004) · Biotechnology Advances · doi:10.1016/j.biotechadv.2004.09.002 · Cited by 244 · see citing works
Thiol/disulfide redox states in signaling and sensing
Go, Y.-M., & Jones, D. P. (2013) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2013.764840 · Cited by 241 · see citing works
Synthesis of Peroxynitrite in a Two-Phase System Using Isoamyl Nitrite and Hydrogen Peroxide
Uppu, R. M., & Pryor, W. A. (1996) · Analytical Biochemistry · doi:10.1006/abio.1996.0162 · Cited by 230 · see citing works
Oxidation of Therapeutic Proteins and Peptides: Structural and Biological Consequences
Torosantucci, R., Schöneich, C., & Jiskoot, W. (2013) · Pharmaceutical Research · doi:10.1007/s11095-013-1199-9 · Cited by 218 · see citing works
Wright, A., Bubb, W. A., Hawkins, C. L., & Davies, M. J. (2002) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2002)0760035sompoe2.0.co2 · Cited by 202 · see citing works
Self-citationThe carbonate radical and related oxidants derived from bicarbonate buffer
Medinas, D. B., Cerchiaro, G., Trindade, D. F., & Augusto, O. (2007) · IUBMB Life · doi:10.1080/15216540701230511 · Cited by 198 · see citing works
The Hydroxyl Radical in Lens Nuclear Cataractogenesis
Fu, S., Dean, R. T., Southan, M., & Truscott, R. J. W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.44.28603 · Cited by 177 · see citing works
Peroxynitrite Reactions and Diffusion in Biology
Radí, R. (1998) · Chemical Research in Toxicology · doi:10.1021/tx980096z · Cited by 172 · see citing works
Charge transfer between tryptophan and tyrosine in proteins
Butler, J., Land, E. J., Prütz, W. A., & Swallow, A. J. (1982) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(82)90173-x · Cited by 158 · see citing works
Ehrenshaft, M., Deterding, L. J., & Mason, R. P. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.08.003 · Cited by 158 · see citing works
Jacob, J. S., Cistola, D. P., Hsu, F., Muzaffar, S., Mueller, D. M., Hazen, S. L., & Heinecke, J. W. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.33.19950 · Cited by 150 · see citing works
Agon, V. V., Bubb, W. A., Wright, A., Hawkins, C. L., & Davies, M. J. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.09.039 · Cited by 146 · see citing works
Self-citationPulse- and Gamma-Radiolysis of Aqueous Solutions of Tryptophan
Armstrong, R. C., & Swallow, A. J. (1969) · Radiation Research · doi:10.2307/3573010 · Cited by 142 · see citing works
Peroxidic intermediates in photosensitized oxygenation of tryptophan derivatives
Saito, I., Matsuura, T., Nakagawa, M., & Hino, T. (1977) · Accounts of Chemical Research · doi:10.1021/ar50117a006 · Cited by 142 · see citing works
Ronsein, G. E., Oliveira, M. C. B., Miyamoto, S., Medeiros, M. H. G., & Di Mascio, P. (2008) · Chemical Research in Toxicology · doi:10.1021/tx800026g · Cited by 142 · see citing works
DiMarco, T., & Giulivi, C. (2006) · Mass Spectrometry Reviews · doi:10.1002/mas.20109 · Cited by 140 · see citing works
Long-range electron transfer between tyrosine and tryptophan in peptides
Faraggi, M., DeFelippis, M. R., & Klapper, M. H. (1989) · Journal of the American Chemical Society · doi:10.1021/ja00196a019 · Cited by 133 · see citing works
Lucchini, V., Prato, M., Scorrano, G., Stivanello, M., & Valle, G. (1992) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/p29920000259 · Cited by 127 · see citing works
Pathophysiological importance of aggregated damaged proteins
Höhn, A., Jung, T., & Grune, T. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.02.028 · Cited by 126 · see citing works
Novel Intra- and Inter-molecular Sulfinamide Bonds in S100A8 Produced by Hypochlorite Oxidation
Raftery, M. J., Yang, Z., Valenzuela, S. M., & Geczy, C. L. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101566200 · Cited by 125 · see citing works
Bohle, D. S., Hansert, B., Paulson, S. C., & Smith, B. D. (1994) · Journal of the American Chemical Society · doi:10.1021/ja00095a062 · Cited by 125 · see citing works
Post-Translational Control of Protein Function by Disulfide Bond Cleavage
Cook, K. M., & Hogg, P. J. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4807 · Cited by 118 · see citing works
Modification of tryptophan and tryptophan residues in proteins by reactive nitrogen species
Yamakura, F., & Ikeda, K. (2005) · Nitric Oxide · doi:10.1016/j.niox.2005.07.009 · Cited by 117 · see citing works
Prütz, W. A., Siebert, F., Butler, J., Land, E. J., Ménèz, A., & Garestier, T. (1982) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(82)90172-8 · Cited by 114 · see citing works
Gunther, M. R., Kelman, D. J., Corbett, J. T., & Mason, R. P. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.27.16075 · Cited by 108 · see citing works
Fu, X., Mueller, D. M., & Heinecke, J. W. (2001) · Biochemistry · doi:10.1021/bi015777z · Cited by 107 · see citing works
Peroxidation of a Specific Tryptophan of Metmyoglobin by Hydrogen Peroxide
DeGray, J. A., Gunther, M. R., Tschirret-Guth, R. A., de Montellano, P. R. O., & Mason, R. P. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.4.2359 · Cited by 107 · see citing works
A valid model for the mechanism of oxidation of tryptophan to formylkynurenine—25 years later
Nakagawa, M., Watanabe, H., Kodato, S., Okajima, H., Hino, T., FLIPPEN, J. L., & Witkop, B. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.11.4730 · Cited by 106 · see citing works
Walden, S. E., & Wheeler, R. A. (1996) · The Journal of Physical Chemistry · doi:10.1021/jp951838p · Cited by 86 · see citing works
Harwood, D. T., Kettle, A. J., & Winterbourn, C. C. (2006) · Biochemical Journal · doi:10.1042/bj20060978 · Cited by 85 · see citing works
The reaction of oxygen with radicals from oxidation of tryptophan and indole-3-acetic acid
Candeias, L. P., Wardman, P., & Mason, R. P. (1997) · Biophysical Chemistry · doi:10.1016/s0301-4622(97)00052-5 · Cited by 78 · see citing works
Prütz, W. A., & Land, E. J. (1979) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553007914551301 · Cited by 76 · see citing works
Peroxynitrous acid: controversy and consensus surrounding an enigmatic oxidant
Koppenol, W. H., Bounds, P. L., Nauser, T., Kissner, R., & Rüegger, H. (2012) · Dalton Transactions · doi:10.1039/c2dt31526b · Cited by 72 · see citing works
Leinisch, F., Mariotti, M., Rykær, M., López‐Alarcón, C., Hägglund, P., & Davies, M. J. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.07.025 · Cited by 70 · see citing works
Self-citationYamakura, F., Matsumoto, T., Fujimura, T., Taka, H., Murayama, K., Imai, T., & Uchida, K. (2001) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/s0167-4838(01)00212-6 · Cited by 69 · see citing works
The azide radical and its reaction with tryptophan and tyrosine
Butler, J., Land, E. J., Swallow, A. J., & Prütz, W. A. (1984) · Radiation Physics and Chemistry (1977) · doi:10.1016/0146-5724(84)90118-3 · Cited by 68 · see citing works
Medinas, D. B., Gozzo, F. C., Santos, L. F. A., Iglesias, A. H., & Augusto, O. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.06.018 · Cited by 67 · see citing works
Pietraforte, D., & Minetti, M. (1997) · Biochemical Journal · doi:10.1042/bj3210743 · Cited by 66 · see citing works
Nakagawa, M., Okajima, H., & Hino, T. (1977) · Journal of the American Chemical Society · doi:10.1021/ja00455a035 · Cited by 64 · see citing works
Hasegawa, H., Suzuki, K., Suzuki, K.-J., Nakaji, S., & Sugawara, K. (2000) · Luminescence · doi:10.1002/1522-7243(200009/10)15:5 · Cited by 62 · see citing works
Anderson, R. F., Denny, W. A., Li, W., Packer, J. E., Tercel, M., & Wilson, W. R. (1997) · The Journal of Physical Chemistry A · doi:10.1021/jp972311a · Cited by 61 · see citing works
Self-citationFormation of formylkynurenine by the action of X-rays on tryptophan in aqueous solution
Jayson, G. G., SCHOLES, G., & Weiss, J. (1954) · Biochemical Journal · doi:10.1042/bj0570386 · Cited by 61 · see citing works
Peroxynitrite-mediated oxidation of plasma fibronectin
Degendorfer, G., Chuang, C. Y., Kawasaki, H., Hammer, A., Malle, E., Yamakura, F., & Davies, M. J. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.06.013 · Cited by 53 · see citing works
Self-citationFang, X., Jin, F., Jin, H., & Sonntag, C. V. (1998) · Journal of the Chemical Society, Perkin Transactions 2 · doi:10.1039/a706979k · Cited by 51 · see citing works
Paviani, V., Queiroz, R. F., Marques, E. F., Mascio, P. D., & Augusto, O. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.07.015 · Cited by 50 · see citing works
Reactivity of peptidyl‐tyrosine to hydroxylation and cross‐linking
Burzio, L. A., & Waite, J. H. (2001) · Protein Science · doi:10.1110/ps.44201 · Cited by 50 · see citing works
Xu, J., Eriksson, S. E., Cebula, M., Sandalova, T., Hedström, E., Pader, I., Cheng, Q., Myers, C. R., Antholine, W. E., Nagy, P., et al. (2015) · Cell Death and Disease · doi:10.1038/cddis.2014.574 · Cited by 49 · see citing works
OH Radical-induced Products of Tyrosine Peptides
Karam, L. R., Dizdaroğlu, M., & Simic, M. G. (1984) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553008414551951 · Cited by 48 · see citing works
Cross-linking methionine and amine residues with reactive halogen species
Ronsein, G. E., Winterbourn, C. C., Mascio, P. D., & Kettle, A. J. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.01.023 · Cited by 46 · see citing works
Coelho, F. R., Iqbal, A., Linares, E., Silva, D. F., Lima, F. S., Cuccovia, I. M., & Augusto, O. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.586370 · Cited by 45 · see citing works
Degendorfer, G., Chuang, C. Y., Hammer, A., Malle, E., & Davies, M. J. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.09.018 · Cited by 42 · see citing works
Self-citationX- and γ-radiolysis of Some Tryptophan Dipeptides
Winchester, R. V., & Lynn, K. R. (1970) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553007014550681 · Cited by 37 · see citing works
Aggregation of α-crystallins in kynurenic acid-sensitized UVA photolysis under anaerobic conditions
Sherin, P. S., Zelentsova, E. A., Sormacheva, E. D., Yanshole, V. V., Duzhak, T. G., & Tsentalovich, Y. P. (2015) · Physical Chemistry Chemical Physics · doi:10.1039/c5cp06693j · Cited by 31 · see citing works
Determination of formic acid in aqueous fermentation broth by head-space gas chromatography
Henderson, M. H. (1982) · Journal of Chromatography A · doi:10.1016/s0021-9673(00)84903-1 · Cited by 29 · see citing works
Protein Oxidation and Proteolytic Degradation General Aspects and Relationship to Cataract Formation
Davies, K. J. A. (1990) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-5730-8_77 · Cited by 27 · see citing works
Radiation induced decomposition of tryptophan in the presence of oxygen
Josimović, L., Janković, I., & Jovanović, S. V. (1993) · Radiation Physics and Chemistry · doi:10.1016/0969-806x(93)90029-t · Cited by 27 · see citing works
Zhang, Y., Benmohamed, R., Zhang, W., Kim, J.-H., Edgerly, C. K., Zhu, Y., Morimoto, R. I., Ferrante, R. J., Kirsch, D. R., & Silverman, R. B. (2012) · ACS Medicinal Chemistry Letters · doi:10.1021/ml3000963 · Cited by 23 · see citing works
Rapid benchtop method of alkaline hydrolysis of proteins
Levine, R. L. (1982) · Journal of Chromatography A · doi:10.1016/s0021-9673(00)84902-x · Cited by 22 · see citing works
Interaction of tryptophan and related compounds with oxygen- and carbon-centered radicals
Свердлов, Р. Л., Бринкевич, С. Д., & Шадыро, О. И. (2014) · Free Radical Research · doi:10.3109/10715762.2014.944181 · Cited by 11 · see citing works
Interaction of tryptophan and its derivatives with oxygen- and nitrogen-centered radicals
Свердлов, Р. Л., Khrishchanovich, A. V., Бринкевич, С. Д., & Шадыро, О. И. (2015) · High Energy Chemistry · doi:10.1134/s0018143915020101 · Cited by 3 · see citing works
Flagged first, then by citations
1 of the 76 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Detection, identification, and quantification of oxidative protein modifications
Hawkins, C. L., & Davies, M. J. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.006217 · Cited by 435 · see citing works
Self-citationSuperoxide Anion Chemistry—Its Role at the Core of the Innate Immunity
Andrés, C. M. C., Pérez de la Lastra, J. M., Andrés Juan, C., Plou, F. J., & Pérez-Lebeña, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031841 · Cited by 342 · see citing works
The Chemistry of Protein Oxidation in Food
Hellwig, M. (2019) · Angewandte Chemie International Edition · doi:10.1002/anie.201814144 · Cited by 259 · see citing works
Photosensitization Reactions of Biomolecules: Definition, Targets and Mechanisms
Baptista, M. S., Cadet, J., Greer, A., & Thomas, A. H. (2021) · Photochemistry and Photobiology · doi:10.1111/php.13470 · Cited by 205 · see citing works
Reactivity and degradation products of tryptophan in solution and proteins
Bellmaine, S. F., Schnellbaecher, A., & Zimmer, A. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.09.002 · Cited by 194 · see citing works
Chemical Stability of Proteins in Foods: Oxidation and the Maillard Reaction
Poojary, M. M., & Lund, M. N. (2021) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-052720-104513 · Cited by 138 · see citing works
Fuentes-Lemus, E., Hägglund, P., López‐Alarcón, C., & Davies, M. J. (2021) · Molecules · doi:10.3390/molecules27010015 · Cited by 99 · see citing works
Self-citationIdentification and characterization of protein cross-links induced by oxidative reactions
Hägglund, P., Mariotti, M., & Davies, M. J. (2018) · Expert Review of Proteomics · doi:10.1080/14789450.2018.1509710 · Cited by 61 · see citing works
Self-citationOxidation of myofibrillar proteins induced by peroxyl radicals: Role of oxidizable amino acids
Dorta, E., Ávila, F., Fuentes-Lemus, E., Fuentealba, D., & López‐Alarcón, C. (2019) · Food Research International · doi:10.1016/j.foodres.2019.108580 · Cited by 56 · see citing works
Silva, E., Barrías, P., Fuentes-Lemus, E., Tirapegui, C., Aspée, A., Carroll, L., Davies, M. J., & López‐Alarcón, C. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.11.026 · Cited by 49 · see citing works
Self-citationCarroll, L., Pattison, D. I., Davies, J. B., Anderson, R. F., Lopez-Alarcon, C., & Davies, M. J. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.02.033 · Cited by 48 · see citing works
Self-citationFuentes-Lemus, E., Silva, E., Leinisch, F., Dorta, E., Lorentzen, L. G., Davies, M. J., & López‐Alarcón, C. (2018) · Food Chemistry · doi:10.1016/j.foodchem.2018.02.090 · Cited by 47 · see citing works
Self-citationSound-driven dissipative self-assembly of aromatic biomolecules into functional nanoparticles
Bhangu, S. K., Bocchinfuso, G., Ashokkumar, M., & Cavalieri, F. (2019) · Nanoscale Horizons · doi:10.1039/c9nh00611g · Cited by 47 · see citing works
Li, Y., Jian, X., Zhou, S., Lu, Y., Zhao, C., Gao, Z., & Song, Y. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b02484 · Cited by 46 · see citing works
Fuentes-Lemus, E., Mariotti, M., Hägglund, P., Leinisch, F., Fierro, A., Silva, E., López‐Alarcón, C., & Davies, M. J. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.08.023 · Cited by 44 · see citing works
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Fuentes-Lemus, E., Silva, E., Barrías, P., Aspée, A., Escobar, E. S., Lorentzen, L. G., Carroll, L., Leinisch, F., Davies, M. J., & López‐Alarcón, C. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.06.005 · Cited by 38 · see citing works
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Hipper, E., Blech, M., Hinderberger, D., Garidel, P., & Kaiser, W. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics14010072 · Cited by 34 · see citing works
Oxidation of human plasma fibronectin by inflammatory oxidants perturbs endothelial cell function
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Self-citationA model to understand type I oxidations of biomolecules photosensitized by pterins
Lorente, C., Serrano, M. P., Vignoni, M., Dántola, M. L., & Thomas, A. H. (2021) · Journal of Photochemistry and Photobiology · doi:10.1016/j.jpap.2021.100045 · Cited by 32 · see citing works
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Photo-induced protein oxidation: mechanisms, consequences and medical applications
Fuentes-Lemus, E., & López-Alarcón, C. (2020) · Essays in Biochemistry · doi:10.1042/ebc20190044 · Cited by 29 · see citing works
Photodynamic inactivation of non-enveloped RNA viruses
Majiya, H., Adeyemi, O. O., Herod, M. R., Stonehouse, N. J., & Millner, P. A. (2018) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2018.10.009 · Cited by 25 · see citing works
Figueroa, J. D., Zárate, A. M., Fuentes-Lemus, E., Davies, M. J., & López‐Alarcón, C. (2020) · RSC Advances · doi:10.1039/d0ra04051g · Cited by 24 · see citing works
Self-citationLudvíková, L., Štacko, P., Sperry, J., & Petr Klán, A. (2018) · The Journal of Organic Chemistry · doi:10.1021/acs.joc.8b01545 · Cited by 23 · see citing works
Paviani, V., de Melo, P. J., Avakin, A., Mascio, P. D., Ronsein, G. E., & Augusto, O. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.08.020 · Cited by 21 · see citing works
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Jiang, S., Hägglund, P., Carroll, L., Rasmussen, L. M., & Davies, M. J. (2021) · Redox Biology · doi:10.1016/j.redox.2021.101925 · Cited by 21 · see citing works
Self-citationFuentes-Lemus, E., Jiang, S., Hägglund, P., & Davies, M. J. (2021) · Food Hydrocolloids · doi:10.1016/j.foodhyd.2021.107060 · Cited by 18 · see citing works
Self-citationEl‐Mansy, M. F., Reidl, C. T., Rahaman, M., Özdi̇nler, P. H., & Silverman, R. B. (2023) · Medicinal Research Reviews · doi:10.1002/med.21974 · Cited by 16 · see citing works
Enhanced nuclear-spin hyperpolarization of amino acids and proteins via reductive radical quenchers
Yang, H., Mecha, M. F., Goebel, C. P., & Cavagnero, S. (2021) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2021.106912 · Cited by 16 · see citing works
Vanichkitrungruang, S., Chuang, C. Y., Hawkins, C. L., & Davies, M. J. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101641 · Cited by 16 · see citing works
Self-citationMarques, E. F., de Medeiros, M. H. G., & Mascio, P. D. (2019) · Journal of Mass Spectrometry · doi:10.1002/jms.4448 · Cited by 15 · see citing works
Zhuravleva, Y. S., & Sherin, P. S. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.06.015 · Cited by 15 · see citing works
Figueroa, J. D., Barroso-Torres, N., Morales, M., Herrera, B., Aranda, M., Dorta, E., & López‐Alarcón, C. (2023) · Foods · doi:10.3390/foods12234360 · Cited by 14 · see citing works
Ávila, F., Ravello, N., Zanocco, A. L., Gamon, L. F., Davies, M. J., & Silva, E. D. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.05.024 · Cited by 14 · see citing works
Self-citationJokumsen, K. V., Huhle, V. H., Hägglund, P., Davies, M. J., & Gamon, L. F. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.04.230 · Cited by 11 · see citing works
Self-citationZamora, R. A., Fuentes-Lemus, E., Barrías, P., Herrera-Morandé, A., Mura, F., Guixé, V., Castro‐Fernández, V., Rojas, T., López‐Alarcón, C., Aguirre, P., et al. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.02.006 · Cited by 10 · see citing works
He, J., Becares, E. R., Thulstrup, P. W., Gamon, L. F., Pedersen, J. N., Otzen, D. E., Gourdon, P. E., Davies, M. J., & Hägglund, P. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101631 · Cited by 9 · see citing works
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Figueroa, J. D., Fuentes-Lemus, E., Dorta, E., Melín, V., Cortés‐Ríos, J., Faúndez, M., Contreras, D., Denicola, A., Álvarez, B., Davies, M. J., et al. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101207 · Cited by 7 · see citing works
Self-citationZhuravleva, Y. S., & Sherin, P. S. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.08.001 · Cited by 7 · see citing works
Dong, J., Huang, C., Guo, S., Xia, Y., Hou, Y., Yang, C., Zhang, X., Jie, J., Zhu, B., & Su, H. (2021) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.1c03380 · Cited by 6 · see citing works
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Jacques, E., Ahumada, M., Rector, B. K., Yousefalizadeh, G., Galaz-Araya, C., Recabarren, R., Stamplecoskie, K. G., Poblete, H., & Alarcon, E. I. (2018) · Nanoscale · doi:10.1039/c8nr04018d · Cited by 5 · see citing works
Jørgensen, S. M., Lorentzen, L. G., Hammer, A., Höefler, G., Malle, E., Chuang, C. Y., & Davies, M. J. (2023) · Redox Biology · doi:10.1016/j.redox.2023.102794 · Cited by 5 · see citing works
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Ramos, L. L. P., Farias, D. R., Olivares-Caro, L., Mitsi, C., Mardones, C., Echeverría, J., Ávila, F., & Gutiérrez, M. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e38837 · Cited by 4 · see citing works
Reyes, J. S., Fuentes-Lemus, E., Aspée, A., Davies, M. J., Monasterio, O., & López‐Alarcón, C. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.02.003 · Cited by 4 · see citing works
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Davies, M. J. (2024) · Redox Biochemistry and Chemistry · doi:10.1016/j.rbc.2024.100032 · Cited by 4 · see citing works
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Hellwig, M. (2019) · Angewandte Chemie · doi:10.1002/ange.201814144 · Cited by 3 · see citing works
Ye, J., Bounds, A., Crumpton, M., Long, M., McDonough, H., Srikhirisawan, I., & Gao, S. (2025) · Biochemistry Research International · doi:10.1155/bri/9638644 · Cited by 3 · see citing works
Savina, E. D., Tsentalovich, Y. P., & Sherin, P. S. (2021) · Russian Chemical Bulletin · doi:10.1007/s11172-021-3350-9 · Cited by 3 · see citing works
Sierens, J., Narimisa, M., Demeestere, K., Heugebaert, T. S. A., Nikiforov, A., Geyter, N. D., & Meulenaer, B. D. (2026) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5c12473 · Cited by 2 · see citing works
Zhang, T., Shi, Y. F., Schwartz, J. R., Zhang, Z., Liskey, S. E., Kloxin, C. J., Saven, J. G., & Pochan, D. J. (2026) · ACS Nano · doi:10.1021/acsnano.5c17943 · Cited by 2 · see citing works
Oxygenation is the main pathway for the reaction between superoxide anion and tryptophan radical
Zhuravleva, Y. S., & Sherin, P. S. (2025) · Journal of Photochemistry and Photobiology A Chemistry · doi:10.1016/j.jphotochem.2025.116571 · Cited by 2 · see citing works
Ignasiak, M. T., Frąckowiak, K., Fuentes-Lemus, E., Hägglund, P., Gamon, L. F., Davies, M. J., Marczak, Ł., & Marciniak, B. (2025) · Redox Biochemistry and Chemistry · doi:10.1016/j.rbc.2025.100050 · Cited by 1 · see citing works
Self-citationMorales, M., Villegas, D., Fierro, A., Aranda, M., Carneiro, M. F. H., Davies, M. J., & López‐Alarcón, C. (2025) · ACS Omega · doi:10.1021/acsomega.5c07535 · Cited by 1 · see citing works
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Muñoz‐Rugeles, L., Alvarez-Idaboy, J. R., Rincón, N. E., & Mejía-ospino, E. (2026) · The Journal of Chemical Physics · doi:10.1063/5.0307155 · Cited by 1 · see citing works
Sierens, J., Verheust, Y. P., Heugebaert, T. S. A., Raes, K., Demeestere, K., Nikiforov, A. Y., Geyter, N. D., & Meulenaer, B. D. (2026) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.6c03539 · Cited by 1 · see citing works
Disproportionation and dimerisation of kynurenic acid under UV light
Morozova, O. B., Zhuravleva, Y. S., Geniman, M. P., Yurkovskaya, A. V., & Sherin, P. S. (2023) · Journal of Photochemistry and Photobiology A Chemistry · doi:10.1016/j.jphotochem.2023.115009 · Cited by 1 · see citing works
Chemical modification of 5-hydroxytryptophan photoinduced by endogenous sensitizers present in skin
Farías, J. J., Lizondo‐Aranda, P., Serrano, M. P., Thomas, A. H., Lhiaubet‐Vallet, V., & Dántola, M. L. (2023) · Dyes and Pigments · doi:10.1016/j.dyepig.2023.111919 · Cited by 1 · see citing works
Galluzzi, F. (2021) · theses.fr (ABES) · doi:10.70675/544c95bfz2ddbz4ecaza12dz64e75d212990 · Cited by 1 · see citing works
Zhao, J., Liu, Y., Xu, Y., & Wang, W. (2020) · Nuclear Science and Techniques · doi:10.1007/s41365-020-00776-9
Dzichenka, Y. U., Horetski, M. S., Faletrov, Y. V., Yantsevich, А. V., Shkumatov, V. M., & Usanov, S. A. (2020) · Doklady of the National Academy of Sciences of Belarus · doi:10.29235/1561-8323-2020-64-5-558-566
Ignasiak, M. T., Frąckowiak, K., Gamon, L. F., Davies, M. J., & Marciniak, B. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4477208
Self-citationGutiérrez, M., Ramos, L. L. P., Reyes, D. M., Olivares-Caro, L., Mitsi, C., Mardones, C., Echeverría, J., & Ávila, F. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4893803
Bactericidal properties of tryptophan and pyrrole solutions irradiated by oxygen radicals
Kitagawa, D., Shimizu, K., Watanabe, T., Shimizu, M., Kato, M., Tanaka, H., Ishikawa, K., Hori, M., & Masafumi, I. T. O. (2026) · Japanese Journal of Applied Physics · doi:10.35848/1347-4065/ae4552
- Authors
- Carroll, L., Pattison, D. I., Davies, J. B., Anderson, R. F., Lopez-Alarcon, C., & Davies, M. J.
- Affiliations
- University of Copenhagen (DK)
- The University of Sydney (AU)
- Australian Nuclear Science and Technology Organisation (AU)
- University of Auckland (NZ)
- Corresponding author
- Davies, Michael J.
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 2017-12
- Volume
- 113
- Pages
- 132-142
- ISSN
- 0891-5849 (ISSN-L)
- OpenAlex
- W2757367618
- Cited by
- 67
- References
- 76
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 6 · 2023: 7 · 2021: 14 · 2020: 9 · 2019: 13 · 2018: 8 · 2017: 1
- FWCI
- 3.46
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- ResearchSpace (University of Auckland) (submittedVersion, cc-by)
- Funders
- Australian Research Council (DP140103116)
- Australian Institute of Nuclear Science and Engineering (ALNGRA14021, ALNGRA15521)
- Fondo Nacional de Desarrollo Científico y Tecnológico (1141142)
- Novo Nordisk Fonden (NNF13OC0004294)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Physical Sciences › Chemistry › Organic Chemistry › Free Radicals and Antioxidants
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Electron Spin Resonance Studies
- Keywords
- tryptophan, radical dimerization, protein oxidation, free radicals, protein aggregation, second-order rate constants, pulse radiolysis, peroxynitrous acid, carbonate radical, superoxide dismutase, bicarbonate, tryptophan-containing peptides
- MeSH terms
- Chromatography, Liquid, Free Radicals, Oxidation-Reduction, Peptides, Proteins, Pulse Radiolysis, Tryptophan, Dimerization, Tandem Mass Spectrometry
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