Alternative skin sensitization prediction and risk assessment using proinflammatory biomarkers, interleukin-1 beta (IL-1β) and inducible nitric oxide synthase (iNOS)

References

• Ade, N., S. Martinozzi-Teissier, M. Pallardy, and F. Rousset. 2006. Activation of U937 cells by contact sensitisers: CD86 expression is independent of apoptosis. J. Immunotoxicol. 3:189–97. doi:10.1080/15476910600978038.
   PubMedGoogle Scholar
• An, S., S. Kim, Y. Huh, T. R. Lee, H. K. Kim, K. L. Park, and H. C. Eun. 2009. Expression of surface markers on the human monocytic leukaemia cell line, THP-1, as indicators for the sensitizing potential of chemicals. Contact Derm. 60:185–92. doi:10.1111/j.1600-0536.2009.01528.x.
   PubMed Web of Science ®Google Scholar
• Aptula, A. O., and D. W. Roberts. 2006. Mechanistic applicability domains for non-animal-based prediction of toxicological end points: General principles and application to reactive toxicity. Chem. Res. Toxicol. 19:1097–105. doi:10.1021/tx0601004.
   PubMed Web of Science ®Google Scholar
• Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245–52. doi:10.1038/32588.
   PubMed Web of Science ®Google Scholar
• Basketter, D. A. 1998. Skin sensitization: Risk assessment. Int. J. Cosmetic Sci. 20:141–50. doi:10.1046/j.1467-2494.1998.171746.x.
   PubMedGoogle Scholar
• Basketter, D. A., and P. Cadby. 2004. Reproducible prediction of contact allergenic potency using the local lymph node assay. Contact Derm. 50:15–17. doi:10.1111/j.0105-1873.2004.00278.x.
   PubMed Web of Science ®Google Scholar
• Basketter, D. A., F. Gerberick, and I. Kimber. 2007. The local lymph node assay and the assessment of relative potency: Status of validation. Contact Derm. 57:70–75. doi:10.1111/j.1600-0536.2007.01141.x.
   PubMed Web of Science ®Google Scholar
• Basketter, D. A., G. F. Gerberick, and I. Kimber. 1998. Strategies for identifying false positive responses in predictive skin sensitization tests. Food Chem. Toxicol. 36:327–33. doi:10.1016/S0278-6915(97)00158-0.
   PubMed Web of Science ®Google Scholar
• Basketter, D. A., G. F. Gerberick, I. Kimber, and S. E. Loveless. 1996. The local lymph node assay: A viable alternative to currently accepted skin sensitization tests. Food Chem. Toxicol. 34:985–97. doi:10.1016/S0278-6915(96)00059-2.
   PubMed Web of Science ®Google Scholar
• Basketter, D. A., N. J. Gilmour, Z. M. Wright, T. Walters, A. Boman, and C. Lidén. 2003. Biocides: Characterization of the allergenic hazard of methylisothiazolinone. J. Toxicol. Cutaneous Ocul. Toxicol. 22:187–99. doi:10.1081/CUS-120026299.
   Web of Science ®Google Scholar
• Basketter, D. A., and I. Kimber. 2001. Predictive testing in contact allergy: Facts and future. Allergy 56:937–43. doi:10.1034/j.1398-9995.2001.00147.x.
   PubMed Web of Science ®Google Scholar
• Basketter, D. A., and I. Kimber. 2006. Predictive test for irritants and allergens and their use in quantitative risk assessment. In Contact Dermatitis, ed. P. J. Frosch, T. Menné, and J. P. Lepoittevin, 179–88. 4th ed. Heidelberg: Springer Verlag.
   Google Scholar
• Basketter, D. A., and E. W. Scholes. 1992. Comparison of the local lymph node assay with the guinea-pig maximization test for the detection of a range of contact allergens. Food Chem. Toxicol. 30:65–69. doi:10.1016/0278-6915(92)90138-B.
   PubMed Web of Science ®Google Scholar
• Bauch, C., S. N. Kolle, T. Ramirez, T. Eltze, E. Fabian, A. Mehling, W. Teubner, B. van Ravenzwaay, and R. Landsiedel. 2012. Putting the parts together: Combining in vitro methods to test for skin sensitizing potentials. Reg. Toxicol. Pharmacol. 63:489–504. doi:10.1016/j.yrtph.2012.05.013.
   PubMed Web of Science ®Google Scholar
• Castañeda, A. R., K. J. Bein, S. Smiley-Jewell, and K. E. Pinkerton. 2017. Fine particulate matter (PM2.5) enhances allergic sensitization in BALB/c mice. J. Toxicol. Environ. Health A 80:197–207. doi:10.1080/15287394.2016.1222920.
   PubMed Web of Science ®Google Scholar
• Choi, S. M., T. H. Roh, D. S. Lim, S. Kacew, H. S. Kim, and B. M. Lee. 2018. Risk assessment of benzalkonium chloride in cosmetic products. J. Toxicol. Environ. Health B 21:8–23. doi:10.1080/10937404.2017.1408552.
   PubMed Web of Science ®Google Scholar
• Christensen, A. D., and C. Haase. 2012. Immunological mechanisms of contact hypersensitivity in mice. APMIS 120:1–27. doi:10.1111/j.1600-0463.2011.02832.x.
   PubMed Web of Science ®Google Scholar
• Corsini, E., V. Galbiati, D. Nikitovic, and A. M. Tsatsakis. 2013. Role of oxidative stress in chemical allergens induced skin cells activation. Food Chem. Toxicol. 61:74–81. doi:10.1016/j.fct.2013.02.038.
   PubMed Web of Science ®Google Scholar
• Corsini, E., M. Mitjans, V. Galbiati, L. Lucchi, C. L. Galli, and M. Marinovich. 2009. Use of IL-18 production in a human keratinocyte cell line to discriminate contact sensitisers from irritants and low molecular weight respiratory allergens. Toxicol. In Vitro 23:789–96. doi:10.1016/j.tiv.2009.04.005.
   PubMed Web of Science ®Google Scholar
• Corsini, E., E. L. Roggen, V. Galbiati, and S. Gibbs. 2016. Alternative approach for potency assessment: In vitro methods. Cosmetics 3:7. doi:10.3390/cosmetics3010007.
   Google Scholar
• Cruz, M. T., B. M. Neves, M. Gonçalo, A. Figueiredo, C. B. Duarte, and M. C. Lopes. 2007. Effect of skin sensitizers on inducible nitric oxide synthase expression and nitric oxide production in skin dendritic cells: Role of different immunosuppressive drugs. Immunopharmacol. Immunotoxicol. 29:225–41. doi:10.1080/08923970701512304.
   PubMed Web of Science ®Google Scholar
• Dillon, S. R., C. Sprecher, A. Hammond, J. Bilsborough, M. Rosenfeld-Franklin, S. R. Presnell, H. S. Haugen, M. Maurer, B. Harder, J. Johnston, et al. 2004. Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nat. Immunol. 5:752–60. doi:10.1038/ni1084.
   PubMed Web of Science ®Google Scholar
• EC (European Commission). 2013. Full EU ban on animal testing for cosmetics enters into force. Brussels, Belgium: Europa EU.
   Google Scholar
• ECETOC (European Centre for Ecotoxicology and Toxicology of Chemicals). 2003a. Contact sensitisation: Classification according to potency. Technical Report No.87. European Centre for Ecotoxicology and Toxicology of Chemicals, Brussels, Belgium. Available at: http://www.ecetoc.org/wp-content/uploads/2014/08/ECETOC-TR-087.pdf
   Google Scholar
• ECETOC (European Centre for Ecotoxicology and Toxicology of Chemicals). 2003b. Contact sensitisation: Classification according to potency: A commentary. Document No. 43. European Centre for Ecotoxicology and Toxicology of Chemicals, Brussels, Belgium. Available at: http://www.ecetoc.org/wp-content/uploads/2014/08/DOC-0431.pdf
   Google Scholar
• ECPA (European Crop Protection Association). 2007. Hexyl Cinnamaldehyde (HCA), Potassium Dichromate (PDC) and Formaldehyde (FRM) evaluation of potential dermal sensitization in the local lymph node assay in the mouse. Study SA 06231. Report by Bayer.
   Google Scholar
• Erkes, D. A., and S. R. Selvan. 2014. Hapten-induced contact hypersensitivity, autoimmune reactions, and tumor regression: Plausibility of mediating antitumor immunity. J. Immunol. Res. 2014:175265. doi:10.1155/2014/394127.
   PubMed Web of Science ®Google Scholar
• Estrada, E., G. Patlewicz, M. Chamberlain, D. Basketter, and S. Larbey. 2003. Computer-aided knowledge generation for understanding skin sensitization mechanisms: The TOPS-MODE approach. Chem. Res. Toxicol. 16:1226–35. doi:10.1021/tx034093k.
   PubMed Web of Science ®Google Scholar
• Galbiati, V., M. Mitjans, L. Lucchi, B. Viviani, C. L. Galli, M. Marinovich, and E. Corsini. 2011. Further development of the NCTC 2544 IL-18 assay to identify in vitro contact allergens. Toxicol. In Vitro 25:724–32. doi:10.1016/j.tiv.2010.12.011.
   PubMed Web of Science ®Google Scholar
• Gamer, A. O., E. Nies, and H. W. Vohr. 2008. Local lymph node assay (LLNA): Comparison of different protocols by testing skin-sensitizing epoxy resin system components. Reg. Toxicol. Pharmacol. 52:290–98. doi:10.1016/j.yrtph.2008.08.018.
   PubMed Web of Science ®Google Scholar
• Gerberick, G. F., R. V. House, E. R. Fletcher, and C. A. Ryan. 1992. Examination of the local lymph node assay for use in contact sensitization risk assessment. Fundam. Appl. Toxicol. 19:438–45. doi:10.1016/0272-0590(92)90183-I.
   PubMedGoogle Scholar
• Gerberick, G. F., M. K. Robinson, C. A. Ryan, R. J. Dearman, I. Kimber, D. A. Basketter, Z. Wright, and J. G. Marks. 2001. Contact allergenic potency: Correlation of human and local lymph node assay data. Am. J. Contact Dermat 12:156–61. doi:10.1053/ajcd.2001.23926.
   PubMedGoogle Scholar
• Gerberick, G. F., C. A. Ryan, P. S. Kern, H. Schlatter, R. J. Dearman, I. Kimber, G. Y. Patlewicz, and D. A. Basketter. 2005. Compilation of historical local lymph node data for evaluation of skin sensitization alternative methods. Dermatitis 16:157–202. doi:10.2310/6620.2005.05040.
   PubMed Web of Science ®Google Scholar
• Gerberick, G. F., J. A. Troutman, L. M. Foertsch, J. D. Vassallo, M. Quijano, R. L. Dobson, C. Goebel, and J. P. Lepoittevin. 2009. Investigation of peptide reactivity of pro-hapten skin sensitizers using a peroxidase-peroxide oxidation system. Toxicol. Sci. 112:164–74. doi:10.1093/toxsci/kfp192.
   PubMed Web of Science ®Google Scholar
• Gerberick, G. F., J. D. Vassallo, R. E. Bailey, J. G. Chaney, S. W. Morrall, and J. P. Lepoittevin. 2004. Development of a peptide reactivity assay for screening contact allergens. Toxicol. Sci. 81:332–43. doi:10.1093/toxsci/kfh213.
   PubMed Web of Science ®Google Scholar
• Gerberick, G. F., J. D. Vassallo, L. M. Foertsch, B. B. Price, J. G. Chaney, and J. P. Lepoittevin. 2007. Quantification of chemical peptide reactivity for screening contact allergens: A classification tree model approach. Toxicol. Sci. 97:417–27. doi:10.1093/toxsci/kfm064.
   PubMed Web of Science ®Google Scholar
• Gibbs, S., I. Kosten, R. Veldhuizen, S. Spiekstra, E. Corsini, E. Roggen, T. Rustemeyer, A. J. Feilzer, and C. J. Kleverlaan. 2018. Assessment of metal sensitizer potency with the reconstructed human epidermis IL-18 assay. Toxicology 393:62–72. doi:10.1016/j.tox.2017.10.014.
   PubMed Web of Science ®Google Scholar
• Ikarashi, Y., K. Ohno, T. Tsuchiya, and A. Nakamura. 1992. Differences of draining lymph node cell proliferation among mice, rats and guinea pigs following exposure to metal allergens. Toxicology 76:283–92. doi:10.1016/0300-483X(92)90196-L.
   PubMed Web of Science ®Google Scholar
• Jin, H., R. He, M. Oyoshi, and R. S. Geha. 2009. Animal models of atopic dermatitis. J. Invest. Dermatol. 129:31–40. doi:10.1038/jid.2008.106.
   PubMed Web of Science ®Google Scholar
• Jo, G. H., S. N. Kim, M. J. Kim, and Y. Heo. 2018. Protective effect of Paeoniae radix alba root extract on immune alterations in mice with atopic dermatitis. J. Toxicol. Environ. Health A. 81:502–11. doi:10.1080/15287394.2018.1460785.
   PubMed Web of Science ®Google Scholar
• Kim, J., J. Lee, S. Shin, A. Cho, and Y. Heo. 2018b. Molecular mechanism of atopic dermatitis induction following sensitization and challenge with 2,4-dinitrochlorobenzene in mouse skin tissue. Toxicol. Res. 34:7–12. doi:10.5487/TR.2018.34.1.007.
   PubMed Web of Science ®Google Scholar
• Kim, M. K., K. B. Kim, K. Yoon, S. Kacew, H. S. Kim, and B. M. Lee. 2018a. IL-1α and IL-1β as alternative biomarkers for risk assessment and the prediction of skin sensitization potency. J. Toxicol. Environ. Health A 81:830–43. doi:10.1080/15287394.2018.1494474.
   PubMed Web of Science ®Google Scholar
• Kimber, I., J. Hilton, P. A. Botham, D. A. Basketter, E. W. Scholes, K. Miller, M. C. Robbins, P. T. Harrison, T. J. Gray, and S. J. Waite. 1991. The murine local lymph node assay: Results of an inter-laboratory trial. Toxicol. Lett. 55:203–13. doi:10.1016/0378-4274(91)90135-S.
   PubMed Web of Science ®Google Scholar
• Kimber, I., and C. Weisenberger. 1991. Anamnestic responses to contact allergens: Application in the murine local lymph node assay. J. Appl. Toxicol. 11:129–33. doi:10.1002/jat.2550110211.
   PubMed Web of Science ®Google Scholar
• Laouini, D., A. Elkhal, A. Yalcindag, S. Kawamoto, H. Oettgen, and R. S. Geha. 2005. COX-2 inhibition enhances the TH2 immune response to epicutaneous sensitization. J. Allergy Clin. Immunol. 116:390–96. doi:10.1016/j.jaci.2005.03.042.
   PubMed Web of Science ®Google Scholar
• Lee, B. M., and S. Kacew. 2018. Advances in toxicological research and risk assessment. J. Toxicol. Environ. Health A 81:240. doi:10.1080/15287394.2018.1439689.
   PubMed Web of Science ®Google Scholar
• Lee, M., J. H. Hwang, and K. M. Lim. 2017. Alternatives to in vivo Draize rabbit eye and skin irritation tests with a focus on 3D reconstructed human cornea-like epithelium and epidermis models. Toxicol. Res. 33:191–203. doi:10.5487/TR.2017.33.3.191.
   PubMed Web of Science ®Google Scholar
• Lim, D. S., S. M. Choi, K. B. Kim, K. Yoon, S. Kacew, H. S. Kim, and B. M. Lee. 2018a. Determination of fragrance allergens and their dermal sensitization quantitative risk assessment (QRA) in 107 spray perfumes. J. Toxicol. Environ. Health A 81:1173–85. doi:10.1080/15287394.2018.1543232.
   PubMed Web of Science ®Google Scholar
• Lim, D. S., T. H. Roh, M. K. Kim, Y. C. Kwon, S. M. Choi, S. J. Kwack, K. B. Kim, S. Yoon, H. S. Kim, and B. M. Lee. 2018b. Non-cancer, cancer, and dermal sensitization risk assessment of heavy metals in cosmetics. J. Toxicol. Environ. Health A 81:432–52. doi:10.1080/15287394.2018.1451191.
   PubMed Web of Science ®Google Scholar
• Montelius, J., H. Wahlkvist, A. Boman, P. Fernström, L. Gråbergs, and J. E. Wahlberg. 1994. Experience with the murine local lymph node assay: Inability to discriminate between allergens and irritants. Acta Derm. Venereol. 74:22–27. doi:10.2340/00015555742227.
   PubMed Web of Science ®Google Scholar
• Mukaka, M. M. 2012. Statistics corner: A guide to appropriate use of correlation coefficient in medical research. Malawi Med. J. 24:69–71.
   PubMed Web of Science ®Google Scholar
• Nepal, M. R., Y. Kang, M. J. Kang, D. H. Nam, and T. C. Jeong. 2018. A β-galactosidase-expressing E. coli culture as an alternative test to identify skin sensitizers and non-sensitizers. J. Toxicol. Environ. Health A 81:288–301. doi:10.1080/15287394.2018.1440187.
   PubMed Web of Science ®Google Scholar
• Novak, N., J. Haberstok, E. Geiger, and T. Bieber. 1999. Dendritic cells in allergy. Allergy 54:792–803.
   PubMed Web of Science ®Google Scholar
• NTP (National Toxicology Program). 1997. Assessment of Contact Hypersensitivity to Dinitrochlorobenzene, Potassium Dichromate and Methyl Salicylate in BALB16 Female Mice. Research Triangle Park, NC: National Institute of Environmental Health Sciences.
   Google Scholar
• Nukada, Y., T. Ashikaga, M. Miyazawa, M. Hirota, H. Sakaguchi, H. Sasa, and N. Nishiyama. 2012. Prediction of skin sensitization potency of chemicals by human cell line activation test (h-CLAT) and an attempt at classifying skin sensitization potency. Toxicol. In Vitro 26:1150–60. doi:10.1016/j.tiv.2012.07.001.
   PubMed Web of Science ®Google Scholar
• OECD (Organisation for Economic Co-operation and Development). 2010. OECD guideline for the testing of chemicals. Skin Sensitization: Local Lymph Node Assay.
   Google Scholar
• OECD (Organisation for Economic Co-operation and Development). 2012a. The adverse outcome pathway for skin sensitisation initiated by covalent binding to proteins part 1: Scientific evidence. Series on Testing and Assessment. No. 168.
   Google Scholar
• OECD (Organisation for Economic Co-operation and Development). 2012b. The adverse outcome pathway for skin sensitisation initiated by covalent binding to proteins. Part 2: Use of the AOP to Develop Chemical Categories and Integrated Assessment and Testing Approaches. Series on Testing and Assessment. No. 168.
   Google Scholar
• Parikh, R., A. Mathai, S. Parikh, G. C. Sekhar, and R. Thomas. 2008. Understanding and using sensitivity, specificity and predictive values. Indian J. Ophthalmol. 56:45–50. doi:10.4103/0301-4738.37595.
   PubMed Web of Science ®Google Scholar
• Park, J., H. Lee, and K. Park. 2018. Mixture toxicity of methylisothiazolinone and propylene glycol at a maximum concentration for personal care products. Toxicol. Res. 34:355–61. doi:10.5487/TR.2018.34.4.355.
   PubMed Web of Science ®Google Scholar
• Python, F., C. Goebel, and P. Aeby. 2007. Assessment of the U937 cell line for the detection of contact allergens. Toxicol. Appl. Pharmacol. 220:113–24. doi:10.1016/j.taap.2006.12.026.
   PubMed Web of Science ®Google Scholar
• Reisinger, K., S. Hoffmann, N. Alépée, T. Ashikaga, J. Barroso, C. Elcombe, N. Gellatly, V. Galbiati, S. Gibbs, H. Groux, et al. 2015. Systematic evaluation of non-animal test methods for skin sensitisation safety assessment. Toxicol. In Vitro 29:259–70. doi:10.1016/j.tiv.2014.10.018.
   PubMed Web of Science ®Google Scholar
• Reuter, H., J. Spieker, S. Gerlach, U. Engels, W. Pape, L. Kolbe, R. Schmucker, H. Wenck, W. Diembeck, K. P. Wittern, et al. 2011. In vitro detection of contact allergens: Development of an optimized protocol using human peripheral blood monocyte-derived dendritic cells. Toxicol. In Vitro 25:315–23. doi:10.1016/j.tiv.2010.09.016.
   PubMed Web of Science ®Google Scholar
• RIFM (Research Institute for Fragrance Materials). 2007. Data submission to NICEATM. (NICEATM, ed). Woodcliff Lake, NJ.
   Google Scholar
• Roggen, E. L. 2014. In vitro approaches for detection of chemical sensitization. Basic Clin. Pharmacol. Toxicol. 115:32–40. doi:10.1111/bcpt.12202.
   PubMed Web of Science ®Google Scholar
• Ross, R., and A. B. Reske-Kunz. 2001. The role of NO in contact hypersensitivity. Int. Immunopharmacol. 1:1469–78. doi:10.1016/S1567-5769(01)00091-1.
   PubMed Web of Science ®Google Scholar
• Ryan, C. A., L. W. Cruse, R. A. Skinner, R. J. Dearman, I. Kimber, and G. F. Gerberick. 2002. Examination of a vehicle for use with water soluble materials in the murine local lymph node assay. Food Chem. Toxicol. 40:1719–25. doi:10.1016/S0278-6915(02)00116-3.
   PubMed Web of Science ®Google Scholar
• Ryan, C. A., G. F. Gerberick, L. W. Cruse, D. A. Basketter, L. Lea, L. Blaikie, R. J. Dearman, E. V. Warbrick, and I. Kimber. 2000. Activity of human contact allergens in the murine local lymph node assay. Contact Derm. 43:95–102. doi:10.1034/j.1600-0536.2000.043002095.x.
   PubMed Web of Science ®Google Scholar
• Saito, K., M. Miyazawa, Y. Nukada, H. Sakaguchi, and N. Nishiyama. 2013. Development of an in vitro skin sensitization test based on ROS production in THP-1 cells. Toxicol. In Vitro 27:857–63. doi:10.1016/j.tiv.2012.12.025.
   PubMed Web of Science ®Google Scholar
• Sakaguchi, H., T. Ashikaga, M. Miyazawa, N. Kosaka, Y. Ito, K. Yoneyama, S. Sono, H. Itagaki, H. Toyoda, and H. Suzuki. 2009. The relationship between CD86/CD54 expression and THP-1 cell viability in an in vitro skin sensitization test human cell line activation test (hCLAT). Cell Biol. Toxicol. 25:109–26. doi:10.1007/s10565-008-9059-9.
   PubMed Web of Science ®Google Scholar
• Schäfer, T., E. Böhler, S. Ruhdorfer, L. Weigl, D. Wessner, B. Filipiak, H. E. Wichmann, and J. Ring. 2001. Epidemiology of contact allergy in adults. Allergy 56:1192–96. doi:10.1034/j.1398-9995.2001.00086.x.
   PubMed Web of Science ®Google Scholar
• Sire, G. 2005. m-Aminophenol (A015): evaluation of skin sensitisation potential in mice using the Local Lymph Node Assay (LLNA). CIT Study No. 26945 TSS.
   Google Scholar
• Toebak, M. J., S. Gibbs, D. P. Bruynzeel, R. J. Scheper, and T. Rustemeyer. 2009. Dendritic cells: Biology of the skin. Contact Derm. 60:2–20. doi:10.1111/j.1600-0536.2008.01443.x.
   PubMed Web of Science ®Google Scholar
• Vocanson, M., M. Cluzel-Tailhardat, G. Poyet, M. Valeyrie, C. Chavagnac, B. Levarlet, P. Courtellemont, A. Rozières, A. Hennino, and J. F. Nicolas. 2008. Depletion of human peripheral blood lymphocytes in CD25+ cells allows for the sensitive in vitro screening of contact allergens. J. Invest. Dermatol. 128:2119–22. doi:10.1038/jid.2008.15.
   PubMed Web of Science ®Google Scholar
• Wright, Z. M., P. A. Basketter, L. Blaikie, K. J. Cooper, E. V. Warbrick, R. J. Dearman, and I. Kimber. 2001. Vehicle effects on skin sensitizing potency of four chemicals: Assessment using the local lymph node assay. Int. J. Cosmetic Sci. 23:75–83. doi:10.1046/j.1467-2494.2001.00066.x.
   PubMedGoogle Scholar