Genes specifically modulated in sensitized skins allow the detection of sensitizers in a reconstructed human skin model. Development of the SENS-IS assay

Toxicology in Vitro

Volumn 29, Issue 4, 2015, Pages 787-802

  Cottrez, Françoise ^a   Boitel, Elodie ^a   Auriault, Claude ^a   Aeby, Pierre ^a   Groux, Hervé ^a  

^a Les Cyclades   (France)

Author keywords

Alternatives to animal tests; Reconstituted epidermis; SENS IS; Skin sensitization; Toxicogenomics

Indexed keywords

1,4 BENZOQUINONE; 2 MERCAPTOBENZOTHIAZOLE; BENZALKONIUM CHLORIDE; BENZOIC ACID; BUTANOL; CINNAMALDEHYDE; CITRAL; DIMETHYL SULFOXIDE; DODECYL SULFATE SODIUM; EUGENOL; FORMALDEHYDE; GALLIC ACID PROPYL ESTER; GLYCEROL; GLYOXAL; HYDROXYCITRONELLAL; LACTIC ACID; MACROGOL; MALEIC ACID DIETHYL ESTER; OCTANOIC ACID; OXAZOLONE; PHENYLENEDIAMINE; PHTHALIC ACID DIETHYL ESTER; POTASSIUM HYDROXIDE; PROPYL PARABEN; PROPYLENE GLYCOL; SALICYLIC ACID; SULFANILIC ACID; TRIMELLITIC ANHYDRIDE; TRINITROBENZENESULFONIC ACID; UNINDEXED DRUG; BIOLOGICAL MARKER; CYSTEINE; GENETIC MARKER; IRRITANT AGENT;

ARE GENE; ARTICLE; BIOASSAY; CONTROLLED STUDY; EPIDERMIS; GENE; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; SENS IS ASSAY; SENS IS GENE; SKIN EXAMINATION; SKIN SENSITIZATION; TOXICOGENETICS; UPREGULATION; ANIMAL; ANIMAL TESTING ALTERNATIVE; CHEMISTRY; DRUG EFFECTS; GENETIC MARKER; MOUSE; PROCEDURES; SKIN; TOXICITY TESTING;

ANIMALIA; MUS;

ANIMAL TESTING ALTERNATIVES; ANIMALS; BIOMARKERS; CYSTEINE; EPIDERMIS; GENE EXPRESSION; GENETIC MARKERS; HUMANS; IRRITANTS; MICE; SKIN; SKIN IRRITANCY TESTS; TOXICOGENETICS;

EID: 84925251177     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2015.02.012     Document Type: Article

References (55)

1. Ade N., Leon F., Pallardy M., Peiffer J.-L., Kerdine-Romer S., Tissier M.-H., Bonnet P.-A., Fabre I., Ourlin J.-C. HMOX1 and NQO1 genes are upregulated in response to contact sensitizers in dendritic cells and THP-1 cell line: role of the Keap1/Nrf2 pathway. Toxicol. Sci. 2009, 107:451-460. 10.1093/toxsci/kfn243.
2. Ade N., Martinozzi-Teissier S., Pallardy M., Rousset F. Activation of U937 cells by contact sensitizers: CD86 expression is independent of apoptosis. J. Immunotoxicol. 2006, 3:189-197. 10.1080/15476910600978038.
3. Aiba S., Terunuma A., Manome H., Tagami H. Dendritic cells differently respond to haptens and irritants by their production of cytokines and expression of co-stimulatory molecules. Eur. J. Immunol. 1997, 27:3031-3038. 10.1002/eji.1830271141.
4. Ainscough J.S., Frank Gerberick G., Dearman R.J., Kimber I. Danger, intracellular signaling, and the orchestration of dendritic cell function in skin sensitization. J. Immunotoxicol. 2013, 10:223-234. 10.3109/1547691X.2012.711782.
5. Ali Z.El, Gerbeix C., Hemon P., Esser P.R., Martin S.F., Pallardy M., Kerdine-Romer S. Allergic skin inflammation induced by chemical sensitizers is controlled by the transcription factor Nrf2. Toxicol. Sci. 2013, 134:39-48. 10.1093/toxsci/kft084.
6. Basketter D.A., Kimber I. Updating the skin sensitization in vitro data assessment paradigm in 2009. J. Appl. Toxicol. 2009, 29:545-550. 10.1002/jat.1443.
7. Basler M., Kirk C.J., Groettrup M. The immunoproteasome in antigen processing and other immunological functions. Curr. Opin. Immunol. 2013, 25:74-80. 10.1016/j.coi.2012.11.004.
8. Casati S., Aeby P., Kimber I., Maxwell G., Ovigne J.M., Roggen E., Rovida C., Tosti L., Basketter D. Selection of chemicals for the development and evaluation of in vitro methods for skin sensitisation testing. Altern. Lab. Anim. 2009, 37:305-312.
9. Chauveau C., Rémy S., Royer P.J., Hill M., Tanguy-Royer S., Hubert F.-X., Tesson L., Brion R., Beriou G., Gregoire M., Josien R., Cuturi M.C., Anegon I. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 2005, 106:1694-1702. 10.1182/blood-2005-02-0494.
10. Corsini E., Mitjans M., Galbiati V., Lucchi L., Galli C.L., Marinovich M. Use of IL-18 production in a human keratinocyte cell line to discriminate contact sensitizers from irritants and low molecular weight respiratory allergens. Toxicol. In Vitro 2009, 23:789-796. 10.1016/j.tiv.2009.04.005.
11. Cotovio J., Grandidier M.-H., Portes P., Roguet R., Rubinstenn G. The in vitro skin irritation of chemicals: optimisation of the EPISKIN prediction model within the framework of the ECVAM validation process. Altern. Lab. Anim. 2005, 33:329-349.
12. Dieng-Kuntz R., Minier D., Růzicka M., Corby F., Corby O., Alamarguy L. Building and using a medical ontology for knowledge management and cooperative work in a health care network. Comput. Biol. Med. 2006, 36:871-892.
13. Emter R., van der Veen J.W., Adamson G., Ezendam J., van Loveren H., Natsch A. Gene expression changes induced by skin sensitizers in the KeratinoSens™ cell line: Discriminating Nrf2-dependent and Nrf2-independent events. Toxicol. In Vitro 2013, 27:2225-2232. 10.1016/j.tiv.2013.09.009.
14. EU, 2003. Directive 2003/15/EC of the European Parliament and the Council of 27 February 2003 Official Journal of the European Union L396, pp. 1-849.
15. EU database downloaded in January 2015 from . http://ec.europa.eu/health/scientific_committees/docs/annex6_respiratory.pdf.
16. Freudenberg M.A., Esser P.R., Jakob T., Galanos C., Martin S.F. Innate and adaptive immune responses in contact dermatitis: analogy with infections. G. Ital. Dermatol. Venereol. 2009, 144:173-185.
17. Gerberick G.F., Vassallo J.D., Foertsch L.M., Price B.B., Chaney J.G., Lepoittevin J.-P. Quantification of chemical peptide reactivity for screening contact allergens: a classification tree model approach. Toxicol. Sci. 2007, 97:417-427. 10.1093/toxsci/kfm064.
18. Hartung T. Comparative analysis of the revised directive 2010/63/EU for the protection of laboratory animals with its predecessor 86/609/EEC - a t4 report. ALTEX 2010, 27:285-303.
19. He T., Quan T., Shao Y., Voorhees J.J., Fisher G.J. Oxidative exposure impairs TGF-β pathway via reduction of type II receptor and SMAD3 in human skin fibroblasts. Age (Dordr) 2014, 36:9623-1094. 10.1007/s11357-014-9623-6.
20. ICCVAM database, downloaded in December 2008 from . http://iccvam.niehs.nih.gov/methods/immunotox/LLNA%20pot/appx/LLNApotencyAppB18Jan08FD.xls.
21. Jain A., Lamark T., Sjøttem E., Larsen K.B., Awuh J.A., Øvervatn A., McMahon M., Hayes J.D., Johansen T. P62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem. 2010, 285:22576-22591. 10.1074/jbc.M110.118976.
22. Jung I.D., Noh K.T., Lee C.-M., Chun S.H., Jeong S.K., Park J.W., Park W.S., Kim H.W., Yun C.-H., Shin Y.K., Park Y.-M. Oncostatin M induces dendritic cell maturation and Th1 polarization. Biochem. Biophys. Res. Commun. 2010, 394:272-278. 10.1016/j.bbrc.2010.02.153.
23. Kagami S., Saeki H., Tsunemi Y., Nakamura K., Kuwano Y., Komine M., Nakayama T., Yoshie O., Tamaki K. CCL27-transgenic mice show enhanced contact hypersensitivity to Th2, but not Th1 stimuli. Eur. J. Immunol. 2008, 38:647-657. 10.1002/eji.200737685.
24. Kim Y.-J., Li G., Broxmeyer H.E. 4-1BB ligand stimulation enhances myeloid dendritic cell maturation from human umbilical cord blood CD34+ progenitor cells. J. Hematother. Stem Cell Res. 2002, 11:895-903. 10.1089/152581602321080556.
25. Kim N., Bae K.B., Kim M.O., Yu D.H., Kim H.J., Yuh H.S., Ji Y.R., Park S.J., Kim S., Son K.-H., Park S.-J., Yoon D., Lee D.-S., Lee S., Lee H.-S., Kim T.-Y., Ryoo Z.Y. Overexpression of cathepsin S induces chronic atopic dermatitis in mice. J. Invest. Dermatol. 2012, 132:1169-1176. 10.1038/jid.2011.404.
26. Kimber I., Travis M.A., Martin S.F., Dearman R.J. Immunoregulation of skin sensitization and regulatory T cells. Contact Derm. 2012, 67:179-183. 10.1111/j.1600-0536.2012.02148.x.
27. Li N., Wang M., Barajas B., Sioutas C., Williams M.A., Nel A.E. Nrf2 deficiency in dendritic cells enhances the adjuvant effect of ambient ultrafine particles on allergic sensitization. J. Innate. Immun. 2013, 5:543-554. 10.1159/000347060.
28. Martin S.F., Esser P.R., Weber F.C., Jakob T., Freudenberg M.A., Schmidt M., Goebeler M. Mechanisms of chemical-induced innate immunity in allergic contact dermatitis. Allergy 2011, 66:1152-1163. 10.1111/j.1398-9995.2011.02652.x.
29. McKim J.M., Keller D.J., Gorski J.R. A new in vitro method for identifying chemical sensitizers combining peptide binding with ARE/EpRE-mediated gene expression in human skin cells. Cutan. Ocul. Toxicol. 2010, 29:171-192. 10.3109/15569527.2010.483869.
30. Moreilhon C., Gras D., Hologne C., Bajolet O., Cottrez F., Magnone V., Merten M., Groux H., Puchelle E., Barbry P. Live staphylococcus aureus and bacterial soluble factors induce different transcriptional responses in human airway cells. Physiol. Genomics 2005, 20:244-255. 10.1152/physiolgenomics.00135.2004.
31. Natsch A., Emter R. Skin sensitizers induce antioxidant response element dependent genes: application to the in vitro testing of the sensitization potential of chemicals. Toxicol. Sci. 2008, 102:110-119.
32. Natsch A., Bauch C., Foertsch L., Gerberick F., Norman K., Hilberer A., Inglis H., Landsiedel R., Onken S., Reuter H., Schepky A., Emter R. The intra- and inter-laboratory reproducibility and predictivity of the KeratinoSens assay to predict skin sensitizers in vitro: results of a ring-study in five laboratories. Toxicol. In Vitro 2011, 25:733-744. 10.1016/j.tiv.2010.12.014.
33. Nosbaum A., Vocanson M., Rozieres A., Hennino A., Nicolas J.-F. Allergic and irritant contact dermatitis. Eur. J. Dermatol. 2009, 19:325-332. 10.1684/ejd.2009.0686.
34. OECD, 2012. 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. ENV/JM/MONO(2012)/PART2.
35. Osawa R., Akiyama M., Shimizu H. Filaggrin gene defects and the risk of developing allergic disorders. Allergol. Int. 2011, 60:1-9. 10.2332/allergolint.10-RAI-0270.
36. Pronk T.E., van Someren E.P., Stierum R.H., Ezendam J., Pennings J.L.A. Unraveling toxicological mechanisms and predicting toxicity classes with gene dysregulation networks. J. Appl. Toxicol. 2013, 33:1407-1415. 10.1002/jat.2800.
37. Python F., Goebel C., Aeby P. Comparative DNA microarray analysis of human monocyte derived dendritic cells and MUTZ-3 cells exposed to the moderate skin sensitizer cinnamaldehyde. Toxicol. Appl. Pharmacol. 2009, 239:273-283.
38. Ramirez T., Mehling A., Kolle S.N., Wruck C.J., Teubner W., Eltze T., Aumann A., Urbisch D., van Ravenzwaay B., Landsiedel R. LuSens: a keratinocyte based ARE reporter gene assay for use in integrated testing strategies for skin sensitization hazard identification. Toxicol. In Vitro 2014, 28:1482-1497. 10.1016/j.tiv.2014.08.002.
39. Reszka E., Jablonowski Z., Wieczorek E., Jablonska E., Krol M.B., Gromadzinska J., Grzegorczyk A., Sosnowski M., Wasowicz W. Polymorphisms of NRF2 and NRF2 target genes in urinary bladder cancer patients. J. Cancer Res. Clin. Oncol. 2014, 140:1723-1731. 10.1007/s00432-014-1733-0.
40. Sakaguchi H., Ashikaga T., Miyazawa M., Kosaka N., Ito Y., Yoneyama K., Sono S., Itagaki H., Toyoda H., Suzuki H. The relationship between CD86/CD54 expression and THP-1 cell viability in an in vitro skin sensitization test-human cell line activation test (h-CLAT). Cell Biol. Toxicol. 2009, 25:109-126. 10.1007/s10565-008-9059-9.
41. Sens-it-iv, 2009. Sens-it-iv Newsletter 32, October, 12, 2009. Downloaded June 2010 from . http://www.sens-it%20iv.eu/files/newsletter/Sens-it-iv_Newsletter_32.html.
42. Sivaprasad U., Kinker K.G., Ericksen M.B., Lindsey M., Gibson A.M., Bass S.A., Hershey N.S., Deng J., Medvedovic M., Khurana Hershey G.K. SERPINB3/B4 contributes to early inflammation and barrier dysfunction in an experimental murine model of atopic dermatitis. J. Invest. Dermatol. 2014, 127(1):254-261.
43. Tokuriki A., Seo N., Ito T., Kumakiri M., Takigawa M., Tokura Y. Dominant expression of CXCR3 is associated with induced expression of IP-10 at hapten-challenged sites of murine contact hypersensitivity: a possible role for interferon-gamma-producing CD8(+) T cells in IP-10 expression. J. Dermatol. Sci. 2002, 28:234-241.
44. Troutman J.A., Foertsch L.M., Kern P.S., Dai H.J., Quijano M., Dobson R.L.M., Lalko J.F., Lepoittevin J.-P., Gerberick G.F. The incorporation of lysine into the peroxidase peptide reactivity assay for skin sensitization assessments. Toxicol. Sci. 2011, 122:422-436. 10.1093/toxsci/kfr101.
45. Uruno A., Motohashi H. The Keap1-Nrf2 system as an in vivo sensor for electrophiles. Nitric Oxide 2011, 25:153-160. 10.1016/j.niox.2011.02.007.
46. van der Veen J.W., Pronk T.E., van Loveren H., Ezendam J. Applicability of a keratinocyte gene signature to predict skin sensitizing potential. Toxicol. In Vitro 2013, 27:314-322. 10.1016/j.tiv.2012.08.023.
47. van der Veen J.W., Soeteman-Hernández L.G., Ezendam J., Stierum R., Kuper F.C., van Loveren H. Anchoring molecular mechanisms to the adverse outcome pathway for skin sensitization: analysis of existing data. Crit. Rev. Toxicol. 2014, 44:590-599. 10.3109/10408444.2014.925425.
48. van der Veen J.W., Hodemaekers H., Reus A.A., Maas W.J.M., van Loveren H., Ezendam J. Human relevance of an in vitro gene signature in HaCaT for skin sensitization. Toxicol. In Vitro 2015, 29:81-84. 10.1016/j.tiv.2014.08.010.
49. van Eijl S., Zhu Z., Cupitt J., Gierula M., Götz C., Fritsche E., Edwards R.J. Elucidation of xenobiotic metabolism pathways in human skin and human skin models by proteomic profiling. PLoS ONE 2012, 7:e41721. 10.1371/journal.pone.0041721.
50. Viola A., Lanzavecchia A. T cell activation determined by T cell receptor number and tunable thresholds. Science 1996, 273:104-106.
51. Wakkach A., Fournier N., Brun V., Breittmayer J.-P., Cottrez F., Groux H. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 2003, 18:605-617.
52. Williams M.A., Rangasamy T., Bauer S.M., Killedar S., Karp M., Kensler T.W., Yamamoto M., Breysse P., Biswal S., Georas S.N. Disruption of the transcription factor Nrf2 promotes pro-oxidative dendritic cells that stimulate Th2-like immunoresponsiveness upon activation by ambient particulate matter. J. Immunol. 2008, 181:4545-4559.
53. Yoshida Y., Sakaguchi H., Ito Y., Okuda M., Suzuki H. Evaluation of the skin sensitization potential of chemicals using expression of co-stimulatory molecules, CD54 and CD86, on the naive THP-1 cell line. Toxicol. In Vitro 2003, 17:221-228.
54. Yusuf N., Nasti T.H., Huang C.-M., Huber B.S., Jaleel T., Lin H.-Y., Xu H., Elmets C.A. Heat shock proteins HSP27 and HSP70 are present in the skin and are important mediators of allergic contact hypersensitivity. J. Immunol. 2009, 182:675-683.
55. Zelenay S., Reis e Sousa C. Adaptive immunity after cell death. Trends Immunol. 2013, 34:329-335. 10.1016/j.it.2013.03.005.