Xenobiotic metabolism gene expression in the EpiDerm™ in vitro 3D human epidermis model compared to human skin

Toxicology in Vitro

Volumn 24, Issue 5, 2010, Pages 1450-1463

  Hu, T ^a   Khambatta, Z S ^a   Hayden, P J ^b   Bolmarcich, J ^b   Binder, R L ^a   Robinson, M K ^a   Carr, G J ^a   Tiesman, J P ^a   Jarrold, B B ^a   Osborne, R ^a   Reichling, T D ^a   Nemeth, S T ^a   Aardema, M J ^a  

^a PROCTER AND GAMBLE COMPANY   (United States)

^b MATTEK CORPORATION   (United States)

Author keywords

EpiDerm 3D human epidermis model; Human skin; Microarray; Xenobiotic metabolism

Indexed keywords

3 METHYLCHOLANTHRENE; ALDEHYDE DEHYDROGENASE; ALDEHYDE OXIDASE; CARBOXYLESTERASE; CYTOCHROME B5 REDUCTASE; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; CYTOCHROME P450 2A6; DIHYDRODIOL DEHYDROGENASE; DIMETHYLANILINE MONOOXYGENASE; EPOXIDE HYDROLASE; ETHOXYRESORUFIN DEETHYLASE; FERREDOXIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCURONOSYLTRANSFERASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HYDROLASE; HYMECROMONE; IDITOL DEHYDROGENASE; KYNURENINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; PROSTACYCLIN; SUPEROXIDE DISMUTASE; THROMBOXANE SYNTHASE;

ARTICLE; BIOTRANSFORMATION; CONTROLLED STUDY; DETOXIFICATION; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INDUCTION; EPIDERMIS; GENE EXPRESSION; GENE INDUCTION; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROARRAY ANALYSIS; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK ASSESSMENT; SKIN; THREE DIMENSIONAL IMAGING; XENOBIOTIC METABOLISM;

ADOLESCENT; BIOTRANSFORMATION; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME INDUCTION; EPIDERMIS; FEMALE; GENE EXPRESSION; GLUCURONOSYLTRANSFERASE; GLUTATHIONE TRANSFERASE; HUMANS; METABOLIC DETOXICATION, DRUG; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SKIN; XENOBIOTICS; YOUNG ADULT;

EID: 77953616112     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2010.03.013     Document Type: Article

References (76)

1. Akintobi A.M., Villano C.M., White L.A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) exposure of normal human dermal fibroblasts results in AhR-dependent and -independent changes in gene expression. Toxicol. Appl. Pharmacol. 2007, 220:9-17.
2. Ashcroft J.-A., Ockendon M., Hotchkiss S.A. Percutaneous absorption of ethanol and detection of the ethanol-metabolizing cytochrome P450 enzyme CYP 2E1 in human skin. Hum. Exp. Toxicol. 1997, 16:400.
3. Baer B.R., Rettie A.E. CYP4B1: an enigmatic P450 at the interface between xenobiotic and endobiotic metabolism. Drug Metab. Rev. 2006, 38:451-476.
4. Cannon C.L., Neal P.J., Southee J.A., Kubilus J., Klausner M. New epidermal model for dermal irritancy testing. Toxicol. In Vitro 1994, 8:889-891.
5. Cheng Z., Radominska-Pandya A., Tephly T.R. Cloning and expression of human UDP-glucuronosyltransferase (UGT) 1A8. Arch. Biochem. Biophys. 1998, 356:301-305.
6. Cheng Z., Radominska-Pandya A., Tephly T.R. Studies on the substrate specificity of human intestinal UDP-glucuronosyltransferases 1A8 and 1A10. Drug Metab. Dispos. 1999, 27:1165-1170.
7. Cheung C., Smith C.K., Hoog J.O., Hotchkiss S.A. Expression and localization of human alcohol and aldehyde dehydrogenase enzymes in skin. Biochem. Biophys. Res. Commun. 1999, 261:100-107.
8. Court M.H., Hazarika S., Krishnaswamy S., Finel M., Williams J.A. Novel polymorphic human UDP-glucuronosyltransferase 2A3: cloning, functional characterization of enzyme variants, comparative tissue expression, and gene induction. Mol. Pharmacol. 2008, 74:744-754.
9. Curren R.D., Mun G.C., Gibson D.P., Aardema M.J. Development of a micronucleus assay in the EpiDerm (TM) human 3D skin model. Environ. Mol. Mutagen. 2004, 44:33.
10. Curren R.D., Mun G.C., Gibson D.P., Aardema M.J. Development of a method for assessing micronucleus induction in a 3D human skin model (EpiDerm). Mutat. Res. 2006, 607:192-204.
11. Dellinger R.W., Fang J.L., Chen G., Weinberg R., Lazarus P. Importance of UDP-glucuronosyltransferase 1A10 (UGT1A10) in the detoxification of polycyclic aromatic hydrocarbons: decreased glucuronidative activity of the UGT1A10139Lys isoform. Drug Metab. Dispos. 2006, 34:943-949.
12. Du L., Neis M.M., Ladd P.A., Lanza D.L., Yost G.S., Keeney D.S. Effects of the differentiated keratinocyte phenotype on expression levels of CYP1-4 family genes in human skin cells. Toxicol. Appl. Pharmacol. 2006, 213:135-144.
13. Duche, D., Luu-The, V., Ferraris, C., Leclaire, J., Labrie, F., 2009. Analysis of Phases 1 and 2 metabolism enzymes in human skin suggests important role of Phase 2 enzymes in the detoxification. The Toxicologist 108 (abstract 1007).
14. Eilstein J., Lereaux G., Daronnat E., Dichich S., Meunier J.R., Leclaire J., Duche D. Characterisation of N-acetyltransferase activity in reconstructed human skin models. Drug Metab. Rev. 2009, 41. (abstract 68).
15. Enayetallah A.E., French R.A., Thibodeau M.S., Grant D.F. Distribution of soluble epoxide hydrolase and of cytochrome P4502C8, 2C9, and 2J2 in human tissues. J. Histochem. Cytochem. 2004, 52:447-454.
16. Falany C.N., He D., Dumas N., Frost A.R., Falany J.L. Human cytosolic sulfotransferase 2B1: isoform expression, tissue specificity and subcellular localization. J. Steroid Biochem. Mol. Biol. 2006, 102:214-221.
17. Flamand N., Marrot L., Belaidi J.P., Bourouf L., Dourille E., Feltes M., Meunier J.R. Development of genotoxicity test procedures with Episkin, a reconstructed human skin model: towards new tools for in vitro risk assessment of dermally applied compounds?. Mutat. Res. 2006, 606:39-51.
18. Foppoli C., De Marco F., Blarzino C., Perluigi M., Cini C., Coccia R. Biological response of human diploid keratinocytes to quinone-producing compounds: role of NAD(P)H: quinone oxidoreductase 1. Int. J. Biochem. Cell Biol. 2005, 37:852-863.
19. Gibbs S., van de Sandt J.J., Merk H.F., Lockley D.J., Pendlington R.U., Pease C.K. Xenobiotic metabolism in human skin and 3D human skin reconstructs: a review. Curr. Drug Metab. 2007, 8:758-772.
20. Goldstein J.A. Clinical relevance of genetic polymorphisms in the human CYP2C subfamily. Br. J. Clin. Pharmacol. 2001, 52:349-355.
21. Gomez-Lechon M.J., Donato T., Jover R., Rodriguez C., Ponsoda X., Glaise D., Castell J.V., Guguen-Guillouzo C. Expression and induction of a large set of drug-metabolizing enzymes by the highly differentiated human hepatoma cell line BC2. Eur. J. Biochem. 2001, 268:1448-1459.
22. Gregory P.A., Gardner-Stephen D.A., Lewinsky R.H., Duncliffe K.N., Mackenzie P.I. Cloning and characterization of the human UDP-glucuronosyltransferase 1A8, 1A9, and 1A10 gene promoters: differential regulation through an interior-like region. J. Biol. Chem. 2003, 278:36107-36114.
23. Gregory P.A., Lewinsky R.H., Gardner-Stephen D.A., Mackenzie P.I. Coordinate regulation of the human UDP-glucuronosyltransferase 1A8, 1A9, and 1A10 genes by hepatocyte nuclear factor 1alpha and the caudal-related homeodomain protein 2. Mol. Pharmacol. 2004, 65:953-963.
24. Harris I.R., Siefken W., Beck-Oldach K., Brandt M., Wittern K.P., Pollet D. Comparison of activities dependent on glutathione S-transferase and cytochrome P-450 IA1 in cultured keratinocytes and reconstructed epidermal models. Skin Pharmacol. Appl. Skin Physiol. 2002, 15(Suppl. 1):59-67.
25. Harris I.R., Siefken W., Beck-Oldach K., Brandt M., Wittern K.P., Pollet D. Comparison of activities dependent on glutathione S-transferase and cytochrome P-450IA1 in cultured keratinocytes and reconstructed epidermal models. Skin Pharmacol. Appl. Skin Physiol. 2002, 15:59-67.
26. Harris I.R., Siefken W., Beck-Oldach K., Wittern K.P., Pollet D. NAD(P)H: quinone reductase activity in human epidermal keratinocytes and reconstructed epidermal models. Skin Pharmacol. Appl. Skin Physiol. 2002, 15:68-73.
27. Hempel N., Gamage N., Martin J.L., McManus M.E. Human cytosolic sulfotransferase SULT1A1. Int. J. Biochem. Cell Biol. 2007, 39:685-689.
28. Higashi Y., Fuda H., Yanai H., Lee Y., Fukushige T., Kanzaki T., Strott C.A. Expression of cholesterol sulfotransferase (SULT2B1b) in human skin and primary cultures of human epidermal keratinocytes. J. Invest. Dermatol. 2004, 122:1207-1213.
29. Hu T., Bailey R.E., Morrall S.W., Aardema M.J., Stanley L.A., Skare J.A. Dermal penetration and metabolism of p-aminophenol and p-phenylenediamine: application of the EpiDerm human reconstructed epidermis model. Toxicol. Lett. 2009, 188:119-129.
30. Hu T., Kaluzhny Y., Mun G.C., Barnett B., Karetsky V., Wilt N., Klausner M., Curren R.D., Aardema M.J. Intralaboratory and interlaboratory evaluation of the EpiDerm 3D human reconstructed skin micronucleus (RSMN) assay. Mutat. Res. 2009, 673:100-108.
31. Janmohamed A., Dolphin C.T., Phillips I.R., Shephard E.A. Quantification and cellular localization of expression in human skin of genes encoding flavin-containing monooxygenases and cytochromes P450. Biochem. Pharmacol. 2001, 62:777-786.
32. Kaluzhny, Y., Karetsky, V., Curren, R.D., Aardema, M.J., Hayden, P., Hu, T., Klausner, M., 2008. Genotoxicity testing using the micronucleus assay in the human EpiDerm™ 3D skin model. The Toxicologist 102 (abstract 883).
33. Katiyar S.K., Matsui M.S., Mukhtar H. Ultraviolet-B exposure of human skin induces cytochromes P450 1A1 and 1B1. J. Invest. Dermatol. 2000, 114:328-333.
34. Kirkland D., Aardema M., Henderson L., Muller L. Evaluation of the ability of a battery of three in vitro genotoxicity tests to discriminate rodent carcinogens and non-carcinogens I. Sensitivity, specificity and relative predictivity. Mutat. Res. 2005, 584:1-256.
35. Klaassen C.D. Casserett and Doull's " Toxicology: The Basic Science of Poisons" 2008, McGraw-Hill.
36. Koukouritaki S.B., Simpson P., Yeung C.K., Rettie A.E., Hines R.N. Human hepatic flavin-containing monooxygenases 1 (FMO1) and 3 (FMO3) developmental expression. Pediatr. Res. 2002, 51:236-243.
37. Luu-The V., Duche D., Ferraris C., Meunier J.R., Leclaire J., Labrie F. Expression profiles of phases 1 and 2 metabolizing enzymes in human skin and the reconstructed skin models Episkin and full thickness model from Episkin. J. Steroid Biochem. Mol. Biol. 2009, 116:178-186.
38. Mastyugin V., Mezentsev A., Zhang W.X., Ashkar S., Dunn M.W., Laniado-Schwartzman M. Promoter activity and regulation of the corneal CYP4B1 gene by hypoxia. J. Cell. Biochem. 2004, 91:1218-1238.
39. Masuda S., Strugnell S.A., Knutson J.C., St-Arnaud R., Jones G. Evidence for the activation of 1alpha-hydroxyvitamin D2 by 25-hydroxyvitamin D-24-hydroxylase: delineation of pathways involving 1alpha, 24-dihydroxyvitamin D2 and 1alpha, 25-dihydroxyvitamin D2. Biochim. Biophys. Acta 2006, 1761:221-234.
40. Merk H., Jugert F., Bonnekoh B., Mahrle G. Induction and inhibition of NAD(P)H: quinone reductase in murine and human skin. Skin Pharmacol. 1991, 4:183-190.
41. Mun G.C., Aardema M.J., Hu T., Barnett B., Kaluzhny Y., Klausner M., Karetsky V., Dahl E.L., Curren R.D. Further development of the EpiDerm 3D reconstructed human skin micronucleus (RSMN) assay. Mutat. Res. 2009, 673:92-99.
42. Murray G.I., Taylor M.C., McFadyen M.C., McKay J.A., Greenlee W.F., Burke M.D., Melvin W.T. Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res. 1997, 57:3026-3031.
43. Naciff J.M., Khambatta Z.S., Thomason R.G., Carr G.J., Tiesman J.P., Singleton D.W., Khan S.A., Daston G.P. The genomic response of a human uterine endometrial adenocarcinoma cell line to 17alpha-ethynyl estradiol. Toxicol. Sci. 2009, 107:40-55.
44. Nohynek G.J., Skare J.A., Meuling W.J.A., Hein D.W., de Bie A., Toutain H. Urinary acetylated metabolites and N-acetyltransferase-2 genotype in human subjects treated with a para-phenylenediamine-containing oxidative hair dye. Food Chem. Toxicol. 2004, 42:1885-1891.
45. Nohynek G.J., Duche D., Garrigues A., Meunier P.A., Toutain H., Leclaire J. Under the skin: biotransformation of para-aminophenol and para-phenylenediamine in reconstructed human epidermis and human hepatocytes. Toxicol. Lett. 2005, 158:196-212.
46. Oesch F., Fabian E., Oesch-Bartlomowicz B., Werner C., Landsiedel R. Drug-metabolizing enzymes in the skin of man, rat, and pig. Drug Metab. Rev. 2007, 39:659-698.
47. Pearse A.D., Marks R. A quantitative histochemical study of three oxidative enzymes in solar keratoses and Bowen's disease. Histochem. J. 1978, 10:621-631.
48. Penning T.M., Burczynski M.E., Jez J.M., Hung C.F., Lin H.K., Ma H., Moore M., Palackal N., Ratnam K. Human 3alpha-hydroxysteroid dehydrogenase isoforms (AKR1C1-AKR1C4) of the aldo-keto reductase superfamily: functional plasticity and tissue distribution reveals roles in the inactivation and formation of male and female sex hormones. Biochem. J. 2000, 351:67-77.
49. Phillips I.R., Shephard E.A. Flavin-containing monooxygenases: mutations, disease and drug response. Trends Pharmacol. Sci. 2008, 29:294-301.
50. Roguet R. The use of reconstructed human epidermis EPISKIN (TM) in the assessment of local tolerance of cosmetics and chemicals. ATLA Altern. Lab. Anim. 2004, 32:83-91.
51. Sadek C.M., Allen-Hoffmann B.L. Cytochrome P450IA1 is rapidly induced in normal human keratinocytes in the absence of xenobiotics. J. Biol. Chem. 1994, 269:16067-16074.
52. Saeki M., Saito Y., Nagano M., Teshima R., Ozawa S., Sawada J.-I. mRNA expression of multiple cytochrome P450 isozymes in four types of cultured skin cells. Int. Arch. Allergy Immunol. 2002, 127:333-336.
53. Sanghani S.P., Quinney S.K., Fredenburg T.B., Davis W.I., Murry D.J., Bosron W.F. Hydrolysis of irinotecan and its oxidative metabolites, 7-ethyl-10-[4-N-(5-aminopentanoic acid)-1-piperidino] carbonyloxycamptothecin and 7-ethyl-10-[4-(1-piperidino)-1-amino]-carbonyloxycamptothecin, by human carboxylesterases CES1A1, CES2, and a newly expressed carboxylesterase isoenzyme, CES3. Drug Metab. Dispos. 2004, 32:505-511.
54. Sanghani S.P., Sanghani P.C., Schiel M.A., Bosron W.F. Human carboxylesterases; an update on CES1, CES2 and CES3. Protein Peptide Lett. 2009, 16:1207-1214.
55. Schafer-Korting M., Bock U., Gamer A., Haberland A., Haltner-Ukomadu E., Kaca M., Kamp H., Kietzmann M., Korting H.C., Krachter H.U., Lehr C.M., Liebsch M., Mehling A., Netzlaff F., Niedorf F., Rubbelke M.K., Schafer U., Schmidt E., Schreiber S., Schroder K.R., Spielmann H., Vuia A. Reconstructed human epidermis for skin absorption testing: results of the German prevalidation study. Altern. Lab. Anim. 2006, 34:283-294.
56. Sit K.H., Lau Y.K., Aw S.E. Differential oxygen sensitivities in G6PDH activities of cultured keloid and normal skin dermis single cells. J. Dermatol. 1991, 18:572-579.
57. Smith C.K., Moore C.A., Elahi E.N., Smart A.T.S., Hotchkiss S.A.M. Human skin absorption and metabolism of the contact allergens, cinnamic aldehyde, and cinnamic alcohol. Toxicol. Appl. Pharmacol. 2000, 168:189-199.
58. Smith G., Dawe R.S., Clark C., Evans A.T., Comrie M.M., Wolf C.R., Ferguson J., Ibbotson S.H. Quantitative real-time reverse transcription-polymerase chain reaction analysis of drug metabolizing and cytoprotective genes in psoriasis and regulation by ultraviolet radiation. J. Invest. Dermatol. 2003, 121:390-398.
59. Smith G., Ibbotson S.H., Comrie M.M., Dawe R.S., Bryden A., Ferguson J., Wolf C.R. Regulation of cutaneous drug-metabolizing enzymes and cytoprotective gene expression by topical drugs in human skin in vivo. Br. J. Dermatol. 2006, 155:275-281.
60. Sonoda J., Xie W., Rosenfeld J.M., Barwick J.L., Guzelian P.S., Evans R.M. Regulation of a xenobiotic sulfonation cascade by nuclear pregnane X receptor (PXR). Proc. Natl. Acad. Sci. USA 2002, 99:13801-13806.
61. Staab C.A., Ceder R., Roberg K., Grafstrom R.C., Hoog J.O. Serum-responsive expression of carbonyl-metabolizing enzymes in normal and transformed human buccal keratinocytes. Cell. Mol. Life Sci. 2008, 65:3653-3663.
62. Stark K., Torma H., Cristea M., Oliw E.H. Expression of CYP4F8 (prostaglandin H 19-hydroxylase) in human epithelia and prominent induction in epidermis of psoriatic lesions. Arch. Biochem. Biophys. 2003, 409:188-196.
63. Stark K., Torma H., Oliw E.H. Co-localization of COX-2, CYP4F8, and mPGES-1 in epidermis with prominent expression of CYP4F8 mRNA in psoriatic lesions. Prostag. Other Lipid Mediat. 2006, 79:114-125.
64. Stark K., Dostalek M., Guengerich F.P. Expression and purification of orphan cytochrome P450 4X1 and oxidation of anandamide. FEBS J. 2008, 275:3706-3717.
65. Strassburg C.P., Manns M.P., Tukey R.H. Expression of the UDP-glucuronosyltransferase 1A locus in human colon. Identification and characterization of the novel extrahepatic UGT1A8. J. Biol. Chem. 1998, 273:8719-8726.
66. Terao M., Kurosaki M., Demontis S., Zanotta S., Garattini E. Isolation and characterization of the human aldehyde oxidase gene: conservation of intron/exon boundaries with the xanthine oxidoreductase gene indicates a common origin. Biochem. J. 1998, 332(Pt 2):383-393.
67. Trasino S.E., Harrison E.H., Wang T.T. Androgen regulation of aldehyde dehydrogenase 1A3 (ALDH1A3) in the androgen-responsive human prostate cancer cell line LNCaP. Exp. Biol. Med. (Maywood) 2007, 232:762-771.
68. Villard P.H., Sampol E., Elkaim J.L., Puyoou F., Casanova D., Seree E., Durand A., Lacarelle B. Increase of CYP1B1 transcription in human keratinocytes and HaCaT cells after UV-B exposure. Toxicol. Appl. Pharmacol. 2002, 178:137-143.
69. Vyas P.M., Roychowdhury S., Koukouritaki S.B., Hines R.N., Krueger S.K., Williams D.E., Nauseef W.M., Svensson C.K. Enzyme-mediated protein haptenation of dapsone and sulfamethoxazole in human keratinocytes: II. Expression and role of flavin-containing monooxygenases and peroxidases. J. Pharmacol. Exp. Ther. 2006, 319:497-505.
70. Wang Y., Rogers P.M., Su C., Varga G., Stayrook K.R., Burris T.P. Regulation of cholesterologenesis by the oxysterol receptor, LXRalpha. J. Biol. Chem. 2008, 283:26332-26339.
71. Welss T., Basketter D.A., Schroder K.R. In vitro skin irritation: facts and future. State of the art review of mechanisms and model. Toxicol. In Vitro 2004, 18:231-243.
72. Williams E.T., Ehsani M.E., Wang X., Wang H., Qian Y.W., Wrighton S.A., Perkins E.J. Effect of buffer components and carrier solvents on in vitro activity of recombinant human carboxylesterases. J. Pharmacol. Toxicol. Meth. 2008, 57:138-144.
73. Xu Z.H., Otterness D.M., Freimuth R.R., Carlini E.J., Wood T.C., Mitchell S., Moon E., Kim U.J., Xu J.P., Siciliano M.J., Weinshilboum R.M. Human 3'-phosphoadenosine 5'-phosphosulfate synthetase 1 (PAPSS1) and PAPSS2: gene cloning, characterization and chromosomal localization. Biochem. Biophys. Res. Commun. 2000, 268:437-444.
74. Yengi L.G., Xiang Q., Pan J., Scatina J., Kao J., Ball S.E., Fruncillo R., Ferron G., Wolf C.R. Quantitation of cytochrome P450 mRNA levels in human skin. Anal. Biochem. 2003, 316:103-110.
75. Zaphiropoulos P.G. Exon skipping and circular RNA formation in transcripts of the human cytochrome P-450 2C18 gene in epidermis and of the rat androgen binding protein gene in testis. Mol. Cell Biol. 1997, 17:2985-2993.
76. Zaphiropoulos P.G. RNA molecules containing exons originating from different members of the cytochrome P450 2C gene subfamily (CYP2C) in human epidermis and liver. Nucl. Acids Res. 1999, 27:2585-2590.