Predicting chemically-induced skin reactions. Part I: QSAR models of skin sensitization and their application to identify potentially hazardous compounds

Toxicology and Applied Pharmacology

Volumn 284, Issue 2, 2015, Pages 262-272

  Alves, Vinicius M ^a,b   Muratov, Eugene ^b,c   Fourches, Denis ^b   Strickland, Judy ^d   Kleinstreuer, Nicole ^d   Andrade, Carolina H ^a   Tropsha, Alexander ^b  

^a FEDERAL UNIVERSITY OF GOIÁS   (Brazil)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c A V BOGATSKY PHYSICO CHEMICAL INSTITUTE   (Ukraine)

^d ILS NTP Interagency Center for the Evaluation of Alternative Toxicological Methods (NICEATM)   (United States)

Author keywords

QSAR; Skin sensitization; Skin toxicants; Virtual screening

Indexed keywords

DANGEROUS GOODS;

BIOLOGICAL MODEL; CHEMICAL MODEL; COMPUTER PROGRAM; DANGEROUS GOODS; DERMATITIS, ALLERGIC CONTACT; DRUG EFFECTS; FACTUAL DATABASE; HUMAN; IMMUNOLOGY; INTOXICATION; QUANTITATIVE STRUCTURE ACTIVITY RELATION; SKIN;

DATABASES, FACTUAL; DERMATITIS, ALLERGIC CONTACT; HAZARDOUS SUBSTANCES; HUMANS; MODELS, CHEMICAL; MODELS, IMMUNOLOGICAL; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; SKIN; SOFTWARE;

EID: 84929366158     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.12.014     Document Type: Article

References (84)

1. Adler S., Basketter D., Creton S., Pelkonen O., van Benthem J., Zuang V., Andersen K.E., Angers-Loustau A., Aptula A., Bal-Price A., Benfenati E., Bernauer U., Bessems J., Bois F.Y., Boobis A., Brandon E., Bremer S., Broschard T., Casati S., Coecke S., Corvi R., Cronin M., Daston G., Dekant W., Felter S., Grignard E., Gundert-Remy U., Heinonen T., Kimber I., Kleinjans J., Komulainen H., Kreiling R., Kreysa J., Leite S.B., Loizou G., Maxwell G., Mazzatorta P., Munn S., Pfuhler S., Phrakonkham P., Piersma A., Poth A., Prieto P., Repetto G., Rogiers V., Schoeters G., Schwarz M., Serafimova R., Tähti H., Testai E., van Delft J., van Loveren H., Vinken M., Worth A., Zaldivar J.-M. Alternative (non-animal) methods for cosmetics testing: current status and future prospects-2010. Arch. Toxicol. 2011, 85:367-485.
2. Aeby P., Ashikaga T., Bessou-Touya S., Schepky A., Gerberick F., Kern P., Marrec-Fairley M., Maxwell G., Ovigne J.-M., Sakaguchi H., Reisinger K., Tailhardat M., Martinozzi-Teissier S., Winkler P. Identifying and characterizing chemical skin sensitizers without animal testing: Colipa's research and method development program. Toxicol. in Vitro 2010, 24:1465-1473.
3. Alves V.M., Muratov E.N., Fourches D., Strickland J., Kleinstreuer N., Andrade C.H., Tropsha A. Predicting chemically-induced skin reactions. Part II: QSAR models of skin permeability and the relationship between skin permeability and skin sensitization. Toxicol. Appl. Pharmacol. 2015, 284:273-280.
4. Anderson S.E., Siegel P.D., Meade B.J. The LLNA: a brief review of recent advances and limitations. J. Allergy 2011, 1-10.
5. Ankley G.T., Bennett R.S., Erickson R.J., Hoff D.J., Hornung M.W., Johnson R.D., Mount D.R., Nichols J.W., Russom C.L., Schmieder P.K., Serrrano J.A., Tietge J.E., Villeneuve D.L. Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ. Toxicol. Chem. 2010, 29:730-741.
6. Artemenko A.G., Muratov E.N., Kuz'min V.E., Muratov N.N., Varlamova E.V., Kuz'mina A.V., Gorb L.G., Golius A., Hill F.C., Leszczynski J., Tropsha A. QSAR analysis of the toxicity of nitroaromatics in Tetrahymena pyriformis: structural factors and possible modes of action. SAR QSAR Environ. Res. 2011, 22:575-601.
7. Basketter D.A., Roberts D.W., Cronin M., Scholes E.W. The value of the local lymph node assay in quantitative structure-activity investigations. Contact Dermatitis 1992, 27:137-142.
8. Basketter D.A., Evans P., Fielder R.J., Gerberick G.F., Dearman R.J., Kimber I. Local lymph node assay - validation, conduct and use in practice. Food Chem. Toxicol. 2002, 40:593-598.
9. Bos J.D., Meinardi M.M. The 500 Dalton rule for the skin penetration of chemical compounds and drugs. Exp. Dermatol. 2000, 9:165-169.
10. Breiman L.E.O. Random Forests. Mach. Learn. 2001, 45:5-32.
11. Breiman L., Friedman J.H., Olshen R.A., Stone C.J. Classification and Regression Trees 1984, Wadsworth Publishing, Belmont.
12. Buehler E.V. Delayed contact hypersensitivity in the guinea pig. Arch. Dermatol. 1965, 91:171-177.
13. Chaudhry Q., Piclin N., Cotterill J., Pintore M., Price N.R., Chrétien J.R., Roncaglioni A. Global QSAR models of skin sensitisers for regulatory purposes. Chem. Cent. J. 2010, 4(Suppl. 1):S5.
14. Chuprina A., Lukin O., Demoiseaux R., Buzko A., Shivanyuk A. Drug- and lead-likeness, target class, and molecular diversity analysis of 7.9million commercially available organic compounds provided by 29 suppliers. J. Chem. Inf. Model. 2010, 50:470-479.
15. Cronin M.T., Basketter D.A. Multivariate QSAR analysis of a skin sensitization database. SAR QSAR Environ. Res. 1994, 2:159-179.
16. Dearman R.J., Wright Z.M., Basketter D.A., Ryan C.A., Gerberick G.F., Kimber I. The suitability of hexyl cinnamic aldehyde as a calibrant for the murine local lymph node assay. Contact Dermatitis 2001, 44:357-361.
17. Dearman R.J., Betts C.J., Farr C., McLaughlin J., Berdasco N., Wiench K., Kimber I. Comparative analysis of skin sensitization potency of acrylates (methyl acrylate, ethyl acrylate, butyl acrylate, and ethylhexyl acrylate) using the local lymph node assay. Contact Dermatitis 2007, 57:242-247.
18. Devillers J. A neural network SAR model for allergic contact dermatitis. Toxicol. Methods 2000, 10:181-193.
19. Dickel H., Kuss O., Schmidt A., Kretz J., Diepgen T.L. Importance of irritant contact dermatitis in occupational skin disease. Am. J. Clin. Dermatol. 2002, 3:283-289.
20. Downs G.M., Barnard J.M. Clustering methods and their uses in computational chemistry. Reviews in Computational Chemistry 2003, 1-40. John Wiley & Sons, Inc., Hoboken. K.B. Lipkowitz, D.B. Boyd (Eds.).
21. ECHA Chlorobenzene [WWW Document] URL, (accessed 5.6.14). http://apps.echa.europa.eu/registered/data/dossiers/DISS-a13af347-47f5-6bef-e044-00144f67d031/AGGR-33e332cc-47ee-4f5c-9167-c351ad8fce8a_DISS-a13af347-47f5-6bef-e044-00144f67d031.html#AGGR-33e332cc-47ee-4f5c-9167-c351ad8fce8a.
22. ECHA Ethylenediamine [WWW Document] URL, (accessed 5.6.14). http://apps.echa.europa.eu/registered/data/dossiers/DISS-9d8437e1-c001-3dc0-e044-00144f67d249/AGGR-adaf1758-e3ff-4e82-ada1-2a36d2b058c8_DISS-9d8437e1-c001-3dc0-e044-00144f67d249.html#AGGR-adaf1758-e3ff-4e82-ada1-2a36d2b058c8.
23. ECHA Oxalic acid [WWW Document] URL, (accessed 5.6.14). http://apps.echa.europa.eu/registered/data/dossiers/DISS-9d952f55-7514-4c7f-e044-00144f67d249/AGGR-9a0763a4-ef26-4d96-a55a-d9ce751e77af_DISS-9d952f55-7514-4c7f-e044-00144f67d249.html#AGGR-9a0763a4-ef26-4d96-a55a-d9ce751e77af.
24. Egeghy P.P., Judson R., Gangwal S., Mosher S., Smith D., Vail J., Hubal E.A.C. The exposure data landscape for manufactured chemicals. Sci. Total Environ. 2012, 414:159-166.
25. Estrada E., Patlewicz G., Chamberlain M., Basketter D., Larbey S. Computer-aided knowledge generation for understanding skin sensitization mechanisms: the TOPS-MODE approach. Chem. Res. Toxicol. 2003, 16:1226-1235.
26. Fourches D., Muratov E., Tropsha A. Trust, but verify: on the importance of chemical structure curation in cheminformatics and QSAR modeling research. J. Chem. Inf. Model. 2010, 50:1189-1204.
27. Gerberick G.F., Vassallo J.D., Bailey R.E., Chaney J.G., Morrall S.W., Lepoittevin J.-P. Development of a peptide reactivity assay for screening contact allergens. Toxicol. Sci. 2004, 81:332-343.
28. Gerberick G.F., Ryan C.A., Kern P.S., Schlatter H. Compilation of historical local lymph node data for evaluation of skin sensitization alternative methods. Dermatitis 2005, 16:157-202.
29. Gerberick G.F., Troutman J.a, Foertsch L.M., Vassallo J.D., Quijano M., Dobson R.L.M., Goebel C., Lepoittevin J.-P. Investigation of peptide reactivity of pro-hapten skin sensitizers using a peroxidase-peroxide oxidation system. Toxicol. Sci. 2009, 112:164-174.
30. Gleeson M.P., Modi S., Bender A., Robinson R.L.M., Kirchmair J., Promkatkaew M., Hannongbua S., Glen R.C. The challenges involved in modeling toxicity data in silico: a review. Curr. Pharm. Des. 2012, 18:1266-1291.
31. Golbraikh A., Tropsha A. Beware of q2!. J. Mol. Graph. Model. 2002, 20:269-276.
32. Golla S., Madihally S., Robinson R.L., Gasem K.A.M. Quantitative structure-property relationship modeling of skin sensitization: a quantitative prediction. Toxicol. in Vitro 2009, 23:454-465.
33. Grandjean P., Berlin A., Gilbert M., Penning W. Preventing percutaneous absorption of industrial chemicals: the "skin" denotation. Am. J. Ind. Med. 1988, 14:97-107.
34. Hennino A., Vocanson M., Chavagnac C., Saint-Mezard P., Dubois B., Kaiserlian D., Nicolas J. Update on the pathophysiology with special emphasis on CD8 effector T cells and CD4 regulatory T cells. An. Bras. Dermatol. 2005, 80:335-347.
35. Hostýnek J.J., Magee P.S. Fragrance allergens: classification and ranking by QSAR. Toxicol. in Vitro 1997, 11:377-384.
36. ICCVAM The reduced murine local lymph node assay: an alternative test method using fewer animals to assess the allergic contact dermatitis potential of chemicals and products [WWW Document] URL, (accessed 2.20.12). http://ntp.niehs.nih.gov/iccvam/docs/immunotox_docs/LLNA-LD/TMER.pdf.
37. ICCVAM, NICEATM The murine local lymph node assay: a test method for assessing the allergic contact dermatitis potential of chemicals/compounds [WWW Document] URL, (accessed 6.8.12). http://iccvam.niehs.nih.gov/docs/immunotox_docs/llna/llnarep.pdf.
38. Jaworska J., Harol A., Kern P.S., Gerberick G.F. Integrating non-animal test information into an adaptive testing strategy - skin sensitization proof of concept case. ALTEX 2011, 28:211-225.
39. Johansson H., Lindstedt M. Prediction of skin sensitizers using alternative methods to animal experimentation. Basic Clin. Pharmacol. Toxicol. 2014, 115:110-117.
40. Johansson H., Lindstedt M., Albrekt A.-S., Borrebaeck C.A.K. A genomic biomarker signature can predict skin sensitizers using a cell-based in vitro alternative to animal tests. BMC Genomics 2011, 12:399.
41. Karlberg A.-T., Bergström M.A., Börje A., Luthman K., Nilsson J.L.G. Allergic contact dermatitis - formation, structural requirements, and reactivity of skin sensitizers. Chem. Res. Toxicol. 2008, 21:53-69.
42. Keegel T., Moyle M., Dharmage S., Frowen K., Nixon R. The epidemiology of occupational contact dermatitis (1990-2007): a systematic review. Int. J. Dermatol. 2009, 48:571-578.
43. Kern P.S., Gerberick G.F., Ryan C.A., Kimber I., Aptula A., Basketter D.A. Local lymph node data for the evaluation of skin sensitization alternatives: a second compilation. Dermatitis 2010, 21:8-32.
44. Kimber I., Basketter D.A., Gerberick G.F., Dearman R.J. Allergic contact dermatitis. Int. Immunopharmacol. 2002, 2:201-211.
45. Kimber I., Basketter D.A., Gerberick G.F., Ryan C.A., Dearman R.J. Chemical allergy: translating biology into hazard characterization. Toxicol. Sci. 2011, 120(S1):S238-S268.
46. Knudsen T.B., Kleinstreuer N.C. Disruption of embryonic vascular development in predictive toxicology. Birth Defects Res. C Embryo Today 2011, 93:312-323.
47. Kuz'min V.E., Artemenko A.G., Muratov E.N., Volineckaya I.L., Makarov V.A., Riabova O.B., Wutzler P., Schmidtke M. Quantitative structure-activity relationship studies of [(biphenyloxy)propyl]isoxazole derivatives. Inhibitors of human rhinovirus 2 replication. J. Med. Chem. 2007, 50:4205-4213.
48. Kuz'min V.E., Artemenko a G., Muratov E.N. Hierarchical QSAR technology based on the Simplex representation of molecular structure. J. Comput. Aided Mol. Des. 2008, 22:403-421.
49. Lepoittevin J.-P. Molecular aspects in allergic and irritant contact dermatitis. Contact Dermatitis 2011, 91-110. Springer, Berlin, Heidelberg. J.D. Johansen, P.J. Frosch, J.-P. Lepoittevin (Eds.).
50. Li S., Fedorowicz A., Singh H., Soderholm S.C. Application of the random forest method in studies of local lymph node assay based skin sensitization data. J. Chem. Inf. Model. 2005, 45:952-964.
51. Low Y., Uehara T., Minowa Y., Yamada H., Ohno Y., Urushidani T., Sedykh A., Muratov E., Kuz'min V., Fourches D., Zhu H., Rusyn I., Tropsha A. Predicting drug-induced hepatotoxicity using QSAR and toxicogenomics approaches. Chem. Res. Toxicol. 2011, 24:1251-1262.
52. Low Y., Sedykh A., Fourches D., Golbraikh A., Whelan M., Rusyn I., Tropsha A. Integrative chemical-biological read-across approach for chemical hazard classification. Chem. Res. Toxicol. 2013, 26:1199-1208.
53. Magee P.S., Hostýnek J.J., Maibach H.I., Francisco S. A classification model for allergic contact dermatitis. QSAR Comb. Sci. 1994, 13:22-33.
54. Maggiora G.M. On outliers and activity cliffs-why QSAR often disappoints. J. Chem. Inf. Model. 2006, 46:1535.
55. Magnusson B., Kligman A.M. The identification of contact allergens by animal assay. The guinea pig maximization test. J. Investig. Dermatol. 1969, 52:268-276.
56. Magnusson B.M., Pugh W.J., Roberts M.S. Simple rules defining the potential of compounds for transdermal delivery or toxicity. Pharm. Res. 2004, 21:1047-1054.
57. Matura M., Sköld M., Börje A., Andersen K.E., Bruze M., Frosch P., Goossens A., Johansen J.D., Svedman C., White I.R., Karlberg A.-T. Selected oxidized fragrance terpenes are common contact allergens. Contact Dermatitis 2005, 52:320-328.
58. Mercier D. Clustering large datasets. Electron. Rev. Linacre Coll. 2003, URL, http://ldc.usb.ve/~mcuriel/Cursos/WC/Transfer.pdf (accessed 6.10.14).
59. Miller M.D., Yourtee D.M., Glaros A.G., Chappelow C.C., Eick J.D., Holder A.J. Quantum mechanical structure-activity relationship analyses for skin sensitization. J. Chem. Inf. Model. 2005, 45:924-929.
60. Muir D.C.G., Howard P.H. Are there other persistent organic pollutants? A challenge for environmental chemists. Environ. Sci. Technol. 2006, 40:7157-7166.
61. Muratov E.N., Artemenko A.G., Varlamova E.V., Polischuk P.G., Lozitsky V.P., Fedchuk A.S., Lozitska R.L., Gridina T.L., Koroleva L.S., Sil'nikov V.N., Galabov A.S., Makarov V.A., Riabova O.B., Wutzler P., Schmidtke M., Kuz'min V.E. Per aspera ad astra: application of Simplex QSAR approach in antiviral research. Future Med. Chem. 2010, 2:1205-1226.
62. Nandy A., Kar S., Roy K. Development of classification- and regression-based QSAR models and in silico screening of skin sensitisation potential of diverse organic chemicals. Mol. Simul. 2014, 40:261-274.
63. OECD OECD principles for the validation, for regulatory purposes, of (Quantitative) Structure-Activity Relationship models [WWW Document] URL, (accessed 4.11.13). http://www.oecd.org/chemicalsafety/risk-assessment/37849783.pdf.
64. OECD Test No. 429: Skin Sensitisation [WWW Document]. OECD Guidelines for the Testing of Chemicals, Section 4: Health Effects URL, (accessed 1.23.13). http://iccvam.niehs.nih.gov/SuppDocs/FedDocs/OECD/OECD-TG429-2010.pdf.
65. OECD The adverse outcome pathway for skin sensitisation initiated by covalent binding to proteins part 1: scientific evidence [WWW Document]. OECD Enviroment, Heal. Safaty Publ URL, (accessed 4.11.12). http://search.oecd.org/officialdocuments/displaydocumentpdf/?cote=env/jm/mono(2012)10/part1&doclanguage=en.
66. OECD OECD QSAR Toolbox v. 3.2 How to use the Toolbox AOP workflow for Skin Sensitization [WWW Document] URL, (accessed 6.10.14). http://www.oecd.org/env/ehs/risk-assessment/Tutorial_1_HowtouseAOPforSkinsensitization_F_28012014.pdf.
67. Polishchuk P.G., Muratov E.N., Artemenko A.G., Kolumbin O.G., Muratov N.N., Kuz'min V.E. Application of random forest approach to QSAR prediction of aquatic toxicity. J. Chem. Inf. Model. 2009, 49:2481-2488.
68. Raunio H. In silico toxicology - non-testing methods. Front. Pharmacol. 2011, 2:33.
69. Roberts D.W., Aptula A.O. Determinants of skin sensitisation potential. J. Appl. Toxicol. 2008, 28:377-387.
70. Roberts D.W., Aptula A.O., Patlewicz G. Electrophilic chemistry related to skin sensitization. Reaction mechanistic applicability domain classification for a published data set of 106 chemicals tested in the mouse local lymph node assay. Chem. Res. Toxicol. 2007, 20:44-60.
71. Roberts D.W., Patlewicz G., Dimitrov S.D., Low L.K., Aptula A.O., Kern P.S., Dimitrova G.D., Comber M.I.H., Phillips R.D., Niemelä J., Madsen C., Wedebye E.B., Bailey P.T., Mekenyan O.G. TIMES-SS-a mechanistic evaluation of an external validation study using reaction chemistry principles. Chem. Res. Toxicol. 2007, 20:1321-1330.
72. Saint-Mezard P., Rosieres A., Berard F., Dubois B., Kaiserlian D., Nicolas J., Krasteva M. Allergic contact dermatitis. Eur. J. Dermatol. 2004, 14:284-295.
73. Schlede E., Aberer W., Fuchs T., Gerner I., Lessmann H., Maurer T., Rossbacher R., Stropp G., Wagner E., Kayser D. Chemical substances and contact allergy-244 substances ranked according to allergenic potency. Toxicology 2003, 193:219-259.
74. Scholes E.W., Basketter D.A., Sarll A.E., Kimber I., Evans C.D., Miller K., Robbins M.C., Harrison P.T., Waite S.J. The local lymph node assay: results of a final inter-laboratory validation under field conditions. J. Appl. Toxicol. 1992, 12:217-222.
75. Scorecard Skin or Sense Organ Toxicants [WWW Document] URL, (accessed 3.3.12). http://scorecard.goodguide.com/health-effects/chemicals-2.tcl?short_hazard_name=skin&all_p=t.
76. Siegel P.D., Fedorowicz A., Butterworth L., Law B., Anderson S.E., Snyder J., Beezhold D. Physical-chemical and solvent considerations in evaluating the influence of carbon chain length on the skin sensitization activity of 1-bromoalkanes. Toxicol. Sci. 2009, 107:78-84.
77. Strid J., Strobel S. Skin barrier dysfunction and systemic sensitization to allergens through the skin. Curr. Drug Targets Inflamm. Allergy 2005, 4:531-541.
78. Todeschini R., Consonni V. Handbook of Molecular Descriptors, Methods and Principles in Medicinal Chemistry 2000, Wiley-VCH, Weinheim, Germany.
79. Tropsha A. Best practices for QSAR model development, validation, and exploitation. Mol. Inform. 2010, 29:476-488.
80. Tropsha A., Golbraikh A. Predictive QSAR modeling workflow, model applicability domains, and virtual screening. Curr. Pharm. Des. 2007, 13:3494-3504.
81. Varnek A., Fourches D., Sieffert N., Solov'ev V.P., Hill C., Lecomte M. QSPR modeling of the Am III/Eu III separation factor: how far can we predict?. Solvent Extr. Ion Exch. 2007, 25:1-26.
82. Varnek A., Fourches D., Horvath D., Klimchuk O., Gaudin C., Vayer P., Solov'ev V., Hoonakker F., Tetko I., Marcou G. ISIDA - platform for virtual screening based on fragment and pharmacophoric descriptors. Curr. Comput. Aided-Drug Des. 2008, 4:191-198.
83. VEGA Skin Sensitization Model v. 2.1.1 [WWW Document] URL, (accessed 6.11.14). http://www.vega-qsar.eu/guidelines/VEGA_model_guide_SKIN_2_1_1.pdf.
84. Watanabe K.H., Andersen M.E., Basu N., Carvan M.J., Crofton K.M., King K.a, Suñol C., Tiffany-Castiglioni E., Schultz I.R. Defining and modeling known adverse outcome pathways: domoic acid and neuronal signaling as a case study. Environ. Toxicol. Chem. 2011, 30:9-21.