Oxidation of a cysteine-derived nucleophilic reagent by dimethyl sulfoxide in the amino acid derivative reactivity assay.
NAC
amino acid derivative reactivity assay (ADRA)
cysteine peptide
dimer
dimethyl sulfoxide (DMSO)
direct peptide reactivity assay (DPRA)
disulfide
in chemico
oxidation
skin sensitization
Journal
Journal of applied toxicology : JAT
ISSN: 1099-1263
Titre abrégé: J Appl Toxicol
Pays: England
ID NLM: 8109495
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
07
11
2019
revised:
22
12
2019
accepted:
27
12
2019
pubmed:
14
2
2020
medline:
13
7
2021
entrez:
14
2
2020
Statut:
ppublish
Résumé
The amino acid derivative reactivity assay (ADRA), which is an in chemico alternative to the use of animals in testing for skin sensitization potential, offers significant advantages over the direct peptide reactivity assay (DPRA) in that it utilizes nucleophilic reagents that are sensitive enough to be used with test chemical solutions prepared to concentrations of 1 mm, which is one-hundredth that of DPRA. ADRA testing of hydrophobic or other poorly soluble compounds requires that they be dissolved in a solvent consisting of dimethyl sulfoxide (DMSO) and acetonitrile. DMSO is known to promote dimerization by oxidizing thiols, which then form disulfide bonds. We investigated the extent to which DMSO oxidizes the cysteine-derived nucleophilic reagents used in both DPRA and ADRA and found that oxidation of both N-(2-(1-naphthyl)acetyl)-l-cysteine (NAC) and cysteine peptide increases as the concentration of DMSO increases, thereby lowering the concentration of the nucleophilic reagent. We also found that use of a solvent consisting of 5% DMSO in acetonitrile consistently lowered NAC concentrations by about 0.4 μm relative to the use of solvents containing no DMSO. We also tested nine sensitizers and four nonsensitizers having different sensitization potencies to compare NAC depletion with and without 5% DMSO and found that reactivity was about the same with either solvent. Based on the above, we conclude that the use of a solvent containing 5% DMSO has no effect on the accuracy of ADRA test results. We plan to review and propose revisions to OECD Test Guideline 442C based on the above investigation.
Substances chimiques
Acetonitriles
0
Irritants
0
Solvents
0
Cysteine
K848JZ4886
Dimethyl Sulfoxide
YOW8V9698H
acetonitrile
Z072SB282N
Types de publication
Comparative Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
843-854Informations de copyright
© 2020 John Wiley & Sons, Ltd.
Références
Aptula, A. O., Patlewicz, G., & Roberts, D. W. (2005). Skin sensitization: Reaction mechanistic applicability domain for structure-activity relationships. Chemical Research in Toxicology, 18, 1420-1426. https://doi.org/10.1021/tx050075m
Aptula, A. O., & Roberts, D. W. (2006). Mechanistic applicability domains for nonanimal-based prediction of toxicological end points: General principles and application to reactive toxicity. Chemical Research in Toxicology, 19, 1097-1105. https://doi.org/10.1021/tx0601004
Bagiyan, G. A., Koroleva, I. K., Soroka, N. V., & Ufimtsev, A. V. (2003). Oxidation of thiol compounds by molecular oxygen in aqueous solutions. Russian Chemical Bulletin, International Edition, 52, 113-1141. https://doi.org/10.1023/A:1024761324710
Bass, R. B., Butler, S. L., Chervitz, S. A., Gloor, S. L., & Falke, J. J. (2007). Use of site-directed cysteine and disulfide chemistry to probe protein structure and dynamics: Applications to soluble and transmembrane receptors of bacterial chemotaxis. Methods in Enzymology, 423, 25-51. https://doi.org/10.1016/S0076-6879(07)23002-2
Cavallini, D., De Marco, C., Duprè, S., & Rotilio, G. (1969). The copper catalyzed oxidation of cysteine to cystine. Archives of Chemistry and Biophysics, 130(1), 354-361. https://doi.org/10.1016/0003-9861(69)90044-7
Cremers, C. M., & Jakob, U. (2013). Oxidant sensing by reversible disulfide bond formation. Journal of Biological Chemistry, 288, 26489-26496. https://doi.org/10.1074/jbc.R113.462929
Ehrenberg, L., Harmsringdahl, M., Fedorcsak, I., & Granath, F. (1989). Kinetics of the copper-catalyzed and iron-catalyzed oxidation of cysteine by dioxygen. Acta Chemica Scandinavica, 43, 177-187. https://doi.org/10.3891/acta.chem.scand.43-0177
Friedman, M. (1973). The chemistry and biochemistry of the sulfhydryl group in amino acids, peptides, and proteins (1st ed.). Oxford, United Kingdom: Pergamon Press.
Fujita, M., Yamamoto, Y., Tahara, H., Kasahara, T., Jimbo, Y., & Hioki, T. (2014). Development of a prediction method for skin sensitization using novel cysteine and lysine derivatives. Journal of Pharmacological and Toxicological Methods, 70(1), 94-105. https://doi.org/10.1016/j.vascn.2014.06.001
Fujita, M., Yamamoto, Y., Wanibuchi, S., Katsuoka, Y., & Kasahara, T. (2019a). The underlying factors that explain why nucleophilic reagents rarely co-elute with test chemicals in the ADRA. Journal of Pharmacological and Toxicological Methods, 96, 95-105. https://doi.org/10.1016/j.vascn.2019.02.004
Fujita, M., Yamamoto, Y., Wanibuchi, S., Katsuoka, Y., & Kasahara, T. (2019b). A newly developed means of HPLC-fluorescence analysis for predicting the skin sensitization potential of multi-constituent substances using ADRA. Toxicology In Vitro, 59, 161-178. https://doi.org/10.1016/j.tiv.2019.04.014
Fujita, M., Yamamoto, Y., Watanabe, S., Sugawara, T., Wakabayashi, K., Tahara, Y., … Kasahara, T. (2019c). The cause of and countermeasures for oxidation of the cysteine-derived reagent used in the amino acid derivative reactivity assay. Journal of Applied Toxicology, 39, 191-208. https://doi.org/10.1002/jat.3707
Fujita, M., Yamamoto, Y., Watanabe, S., Sugawara, T., Wakabayashi, K., Tahara, Y., … Ono, A. (2019d). The within- and between-laboratory reproducibility and predictive capacity of the in chemico Amino acid Derivative Reactivity Assay (ADRA): Results of validation study implemented in four participating laboratories. Journal of Applied Toxicology, 39, 1492-1505. https://doi.org/10.1002/jat.3834
Gerberick, G. F., Vassallo, J. D., Bailey, R. E., Chaney, J. G., Morrall, S. W., & Lepoittevin, J. P. (2004). Development of a peptide reactivity assay for screening contact allergens. Toxicological Sciences, 81(2), 332-343. https://doi.org/10.1093/toxsci/kfh213
Gerberick, G. F., Vassallo, J. D., Foertsch, L. M., Price, B. B., Chaney, J. G., & Lepoittevin, J. P. (2007). Quantification of chemical peptide reactivity for screening contact allergens: a classification tree model approach. Toxicological Sciences, 97(2), 417-427. https://doi.org/10.1093/toxsci/kfm064
Harrison, D. C. (1924). The catalytic action of traces of iron on the oxidation of cysteine and glutathione. Biochemical Journal, 18(5), 1009-1022. https://doi.org/10.1042/bj0181009
Amino acid Derivative Reactivity Assay (ADRA) (2018). JaCVAM Validation Study Report version 1.2 July. Available at http://www.oecd.org/env/ehs/testing/latestdocuments/JaCVAMValidationStudyReportver.1.2(appendix).pdf
Linke, K., & Jakob, U. (2003). Not every disulfide lasts forever: disulfide bond formation as a redox switch. Antioxidants & Redox Signaling, 5, 425-434. https://doi.org/10.1089/152308603768295168
Liu, S., Zhou, L., Chen, L., Dastidar, S. G., Verma, C., Li, J., … Beuerman, R. (2009). Effect of structural parameters of peptides on dimer formation and highly oxidized side products in the oxidation of thiols of linear analogues of human beta-defensin 3 by DMSO. Journal of Peptide Science, 15(2), 95-106. https://doi.org/10.1002/psc.1100
Mannhold, R., Kubinyi, H., & Folkes, G. (2008). Molecular drug properties: Measurement and Prediction. Hoboken, New Jersey, USA: John Wiley & Sons.
Meldrum, N. U., & Dixon, M. (1930). The properties of pure glutathione. Biochemical Journal, 24, 472-496. https://doi.org/10.1042/bj0240472
Michaelis, L., & Flexner, L. B. (1928). Oxidation-reduction systems of biological significance: I. The reduction potential of cysteine: its measurement and significance. Journal of Biological Chemistry, 79, 689-722.
Nagy, P. (2013). Kinetics and mechanisms of thiol-disulfide exchange covering direct substitution and thiol oxidation-mediated pathways. Antioxidants & Redox Signaling, 18(13), 1623-1641. https://doi.org/10.1089/ars.2012.4973
Oae, S. (1991). In J. T. Doi (Ed.), Organic sulfur chemistry: Structure and mechanism (pp. 203-281). Boca Raton: CRC Press.
OECD. (2019a). Test No. 442C APPENDIX II: In Chemico Skin Sensitisation: Amino acid Derivative Reactivity Assay (ADRA). Available at: https://www.oecd-ilibrary.org/docserver/9789264229709-en.pdf?expires=1571962630&id=id&accname=guest&checksum=8A9054AFA2D7E821ACF1F2DE99F077BC
OECD. (2019b). Test No. 442C APPENDIX I: In Chemico Skin Sensitisation: Direct Peptide Reactivity Assay (DPRA). Available at: https://www.oecd-ilibrary.org/docserver/9789264229709-en.pdf?expires=1571962630&id=id&accname=guest&checksum=8A9054AFA2D7E821ACF1F2DE99F077BC
Otaka, A., Koide, T., Shide, A., & Fujii, N. (1991). Application of dimethyl sulphoxide (DMSO)/trifluoroacetic acid (TFA) oxidation to the synthesis of cystine-containing peptide. Tetrahedron Letters, 32(9), 1223-1226. https://doi.org/10.1016/S0040-4039(00)92050-1
Papanyan, Z., & Markarian, S. (2013). Detection of oxidation of L-cysteine by dimethyl sulfoxide in aqueous solutions by IR spectroscopy. Journal of Applied Spectroscopy, 80(5), 775-778. https://doi.org/10.1007/s10812-013-9841-1
Rehder, D. S., & Borges, C. R. (2010). Cysteine sulfenic acid as an intermediate in disulfide bond formation and nonenzymatic protein folding. Biochemistry, 49, 7748-7755. https://doi.org/10.1021/bi1008694
Roberts, D. W., Patlewicz, G., Kern, P. S., Gerberick, F., Kimber, I., Dearman, R. J., … Aptula, A. O. (2007). Mechanistic application domain classification of a Local Lymph Node Assay dataset for skin sensitization. Chemical Research in Toxicology, 20, 1019-1030. https://doi.org/10.1021/tx700024w
Santana-Casiano, J. M., González-Dávila, M., Rodríguez, M. J., & Millero, F. J. (2000). The effect of organic compounds in the oxidation kinetics of Fe(II). Marine Chemistry, 70, 211-222. https://doi.org/10.1016/S0304-4203(00)00027-X
Snow, J. T., Finley, J. W., & Friedman, M. (1975). Oxidation of sulfhydryl groups to disulfides by sulfoxides. Biochemical and Biophysical Research Communications, 64(1), 441-447. https://doi.org/10.1016/0006-291x(75)90272-7
Tam, J. P., Wu, C. R., Liu, W., & Zhang, J. W. (1991). Disulfide bond formation in peptides by dimethyl sulfoxide. Scope and applications. Journal of the American Chemical Society, 113(17), 6657-6662. https://doi.org/10.1021/ja00017a044
Voegtlin, C., Johnson, J. M., & Rosenthal, S. M. (1931). The oxidation catalysis of crystalline glutathione with particular reference to copper. Journal of Biological Chemistry, 93, 435-453.
Wallace, T. J. (1964). Reactions of thiols with sulfoxides. I. Scope of the reaction and synthetic applications. Journal of the American Chemical Society, 86(10), 2018-2021. https://doi.org/10.1021/ja01064a022
Wallace, T. J., & Mahon, J. J. (1964). Reactions of thiols with sulfoxides. II. Kinetics and mechanistic implications. Journal of the American Chemical Society, 86, 4099-4103. https://doi.org/10.1021/ja01073a039
Wanibuchi, S., Yamamoto, Y., Sato, A., Kasahara, T., & Fujita, M. (2019). The Amino Acid Derivative Reactivity Assay with fluorescence detection and its application to multi-constituent substances. The Journal of Toxicological Sciences, 44(12), 821-832. https://doi.org/10.1016/j.vascn.2019.106624
Winther, J. R., & Thorpe, C. (2014). Quantification of thiols and disulfides. Biochimica et Biophysica Acta, 1840(2), 838-846. https://doi.org/10.1016/j.bbagen.2013.03.031
Yamamoto, Y., Fujita, M., Wanibuchi, S., Katsuoka, Y., Ono, A., & Kasahara, T. (2019). Expanding the applicability of the amino acid derivative reactivity assay: Determining a weight for preparation of test chemical solutions that yield a predictive capacity identical to the conventional method using molar concentration and demonstrating the capacity to detect sensitizers in liquid mixtures. Journal of Pharmacological and Toxicological Methods, 97, 67-79. https://doi.org/10.1016/j.vascn.2019.01.001
Yamamoto, Y., Fujita, M., Wanibuchi, S., Sato, A., Akimoto, M., Katsuoka, Y., … Kasahara, T. (2019). Applicability of amino acid derivative reactivity assay for prediction of skin sensitization by combining multiple alternative methods to evaluate key events. The Journal of Toxicological Sciences, 44(9), 585-600. https://doi.org/10.2131/jts.44.585
Yamamoto, Y., Tahara, H., Usami, R., Kasahara, T., Jimbo, Y., Hioki, T., & Fujita, M. (2015). A novel in chemico method to detect skin sensitizers in highly diluted reaction conditions. Journal of Applied Toxicology, 35(11), 1348-1360. https://doi.org/10.1002/jat.3139
Yamamoto, Y., Wanibuchi, S., Sato, A., Kasahara, T., & Fujita, M. (2019). Precipitation of test chemicals in reaction solutions used in the amino acid derivative reactivity assay and the direct peptide reactivity assay. Journal of Pharmacological and Toxicological Methods, 100, 106624. https://doi.org/10.1016/j.vascn.2019.106624