Genetic and pharmacological analysis identifies a physiological role for the AHR in epidermal differentiation

Journal of Investigative Dermatology

Volumn 135, Issue 5, 2015, Pages 1320-1328

  Van Den Bogaard, Ellen H ^a   Podolsky, Michael A ^b   Smits, Jos P ^a   Cui, Xiao ^b   John, Christian ^b   Gowda, Krishne ^c   Desai, Dhimant ^c   Amin, Shantu G ^c   Schalkwijk, Joost ^a   Perdew, Gary H ^b   Glick, Adam B ^b,c  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BLOCKING AGENT; CYTOCHROME P450 1A1; 2-METHYL-2H-PYRAZOLE-3-CARBOXYLIC ACID (2-METHYL-4-O-TOLYLAZOPHENYL)AMIDE; ALLYL COMPOUND; AZO COMPOUND; INDAZOLE DERIVATIVE; INDOLE DERIVATIVE; N-(2-(3H-INDOL-3-YL)ETHYL)-9-ISOPROPYL-2-(5-METHYL-3-PYRIDYL)PURIN-6-AMINE; PURINE DERIVATIVE; PYRAZOLE DERIVATIVE; SGA 360;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG ANALYSIS; EPIDERMIS CELL; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKINFOLD THICKNESS; STRATUM CORNEUM; TRANSCRIPTOMICS; ANIMAL; ANIMAL MODEL; CELL ADHESION; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; EPIDERMIS; GENETICS; KNOCKOUT MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ALLYL COMPOUNDS; ANIMALS; AZO COMPOUNDS; CELL ADHESION; CELL DIFFERENTIATION; CELLS, CULTURED; EPIDERMIS; HUMANS; INDAZOLES; INDOLES; KERATINOCYTES; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; PURINES; PYRAZOLES; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION;

EID: 84928426915     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2015.6     Document Type: Article

References (67)

1. Andersen B, Weinberg WC, Rennekampff O et al. (1997) Functions of the POU domain genes Skn-1a/i and Tst-1/Oct-6/SCIP in epidermal differentiation. Genes Dev 11:1873-84
2. Balato A, Lembo S, Mattii M et al. (2012) IL-33 is secreted by psoriatic keratinocytes and induces pro-inflammatory cytokines via keratinocyte and mast cell activation. Exp Dermatol 21:892-4
3. Boitano AE, Wang J, Romeo R et al. (2010) Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329:1345-8
4. Cameron GS, Baldwin JK, Jasheway DW et al. (1990) Arachidonic acid metabolism varies with the state of differentiation in density gradientseparated mouse epidermal cells. J Invest Dermatol 94:292-6
5. Carrier Y, Ma HL, Ramon HE et al. (2011) Inter-regulation of Th17 cytokines and the IL-36 cytokines in vitro and in vivo: implications in psoriasis pathogenesis. J Invest Dermatol 131:2428-37
6. Cheng C, Kilkenny AE, Roop D et al. (1990) The v-ras oncogene inhibits the expression of differentiation markers and facilitates expression of cytokeratins 8 and 18 in mouse keratinocytes. Mol Carcinog 3:363-73
7. Chiaro CR, Morales JL, Prabhu KS et al. (2008a) Leukotriene A4 metabolites are endogenous ligands for the Ah receptor. Biochemistry 47:8445-55
8. Chiaro CR, Patel RD, Perdew GH (2008b) 12(R)-Hydroxy-5(Z), 8(Z), 10(E), 14(Z)- eicosatetraenoic acid [12(R)-HETE], an arachidonic acid derivative, is an activator of the aryl hydrocarbon receptor. Mol Pharmacol 74:1649-56
9. Choi EY, Lee H, Dingle RW et al. (2012) Development of novel CH223191- based antagonists of the aryl hydrocarbon receptor. Mol Pharmacol 81:3-11
10. Davarinos NA, Pollenz RS (1999) Aryl hydrocarbon receptor imported into the nucleus following ligand binding is rapidly degraded via the cytosplasmic proteasome following nuclear export. J Biol Chem 274:28708-15
11. DiMeglio P, Duarte JH, Ahlfors H et al. (2014) Activation of the aryl hydrocarbon receptor dampens the severity of inflammatory skin conditions. Immunity 40:989-1001
12. DiNatale BC, Schroeder JC, Perdew GH (2010) Ah receptor antagonism inhibits constitutive and cytokine inducible IL6 production in head and neck tumor cell lines. Mol Carcinog 50:173-83
13. Evans CB, Pillai S, Goldyne ME (1993) Endogenous prostaglandin E2 modulates calcium-induced differentiation in human skin keratinocytes. Prostaglandins Leukot Essent Fatty Acids 49:777-81
14. Fernandez-Salguero PM, Ward JM, Sundberg JP et al. (1997) Lesions of arylhydrocarbon receptor-deficient mice. Vet Pathol 34:605-14
15. Forrester AR, Elias MS, Woodward EL et al. (2014) Induction of a chloracne phenotype in an epidermal equivalent model by 2, 3, 7, 8-tetrachlorodibenzo- p-dioxin (TCDD) is dependent on aryl hydrocarbon receptor activation and is not reproduced by aryl hydrocarbon receptor knock down. J Dermatol Sci 73:10-22
16. Fritsche E, Schafer C, Calles C et al. (2007) Lightening up the UV response by identification of the arylhydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation. Proc Natl Acad Sci USA 104:8851-6
17. Geng S, Mezentsev A, Kalachikov S et al. (2006) Targeted ablation of Arnt in mouse epidermis results in profound defects in desquamation and epidermal barrier function. J Cell Sci 119:4901-12
18. Geusau A, Khorchide M, Mildner M et al. (2005) 2, 3, 7, 8-tetrachlorodibenzo-pdioxin impairs differentiation of normal human epidermal keratinocytes in a skin equivalent model. J Invest Dermatol 124:275-7
19. Greenlee WF, Dold KM, Osborne R (1985) Actions of 2, 3, 7, 8-tetrachlorodibenzo- p-dioxin (TCDD) on human epidermal keratinocytes in culture. In Vitro Cell Dev Biol 21:509-12
20. Hogan KA, Ravindran A, Podolsky MA et al. (2013) The TGFbeta1 pathway is required for NFkappaB dependent gene expression in mouse keratinocytes. Cytokine 64:652-9
21. Huang dW, Sherman BT, Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1-13
22. Huang dW, Sherman BT, Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57
23. Hueber AJ, ves-Filho JC, Asquith DL et al. (2011) IL-33 induces skin inflammation with mast cell and neutrophil activation. Eur J Immunol 41:2229-37
24. Ikuta T, Eguchi H, Tachibana T et al. (1998) Nuclear localization and export signals of the human aryl hydrocarbon receptor. J Biol Chem 273: 2895-904
25. Ikuta T, Tachibana T, Watanabe J et al. (2000) Nucleocytoplasmic shuttling of the aryl hydrocarbon receptor. J Biochem 127:503-9
26. Jones CL, Reiners JJ Jr. (1997) Differentiation status of cultured murine keratinocytes modulates induction of genes responsive to 2, 3, 7, 8-tetrachlorodibenzo- p-dioxin. Arch Biochem Biophys 347:163-73
27. Kalmes M, Hennen J, Clemens J et al. (2011) Impact of aryl hydrocarbon receptor (AhR) knockdown on cell cycle progression in human HaCaT keratinocytes. Biol Chem 392:643-51
28. Kumari S, Bonnet MC, Ulvmar MH et al. (2013) Tumor necrosis factor receptor signaling in keratinocytes triggers interleukin-24-dependent psoriasis-like skin inflammation in mice. Immunity 39:899-911
29. Kunz S, Wolk K, Witte E et al. (2006) Interleukin (IL)-19, IL-20 and IL-24 are produced by and act on keratinocytes and are distinct from classical ILs. Exp Dermatol 15:991-1004
30. Lahoti TS, John K, Hughes JM et al. (2013) Aryl hydrocarbon receptor antagonism mitigates cytokine-mediated inflammatory signalling in primary human fibroblast-like synoviocytes. Ann Rheum Dis 72:1708-16
31. Larson RP, Zimmerli SC, Comeau MR et al. (2010) Dibutyl phthalate-induced thymic stromal lymphopoietin is required for Th2 contact hypersensitivity responses. J Immunol 184:2974-84
32. Leong J, Hughes-Fulford M, Rakhlin N et al. (1996) Cyclooxygenases in human and mouse skin and cultured human keratinocytes: association of COX-2 expression with human keratinocyte differentiation. Exp Cell Res 224:79-87
33. Loertscher JA, Sattler CA, len-Hoffmann BL (2001) 2, 3, 7, 8-Tetrachlorodibenzop- dioxin alters the differentiation pattern of human keratinocytes in organotypic culture. Toxicol Appl Pharmacol 175:121-9
34. Markell LM, Masiuk KE, Blazanin N et al. (2011) Pharmacologic inhibition of ALK5 causes selective induction of terminal differentiation in mouse keratinocytes expressing oncogenic HRAS. Mol Cancer Res 9:746-56
35. Muenyi CS, Carrion SL, Jones LA et al. (2014) Effects of in utero exposure of C57BL/6J mice to 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin on epidermal permeability barrier development and function. Environ Health Perspect 122:1052-8
36. Murray IA, Flaveny CA, DiNatale BC et al. (2010a) Antagonism of aryl hydrocarbon receptor signaling by 6, 2', 4'-trimethoxyflavone. J Pharmacol Exp Ther 332:135-44
37. Murray IA, Krishnegowda G, DiNatale BC et al. (2010b) Development of a selective modulator of aryl hydrocarbon (Ah) receptor activity that exhibits anti-inflammatory properties. Chem Res Toxicol 23:955-66
38. Omiecinski CJ, Vanden Heuvel JP, Perdew GH et al. (2010) Xenobiotic metabolism, disposition and regulation by receptors: from biochemical phenomenon to predictors of major toxicities. Toxicol Sci 120(Suppl 1): S49-75
39. Patel RD, Murray IA, Flaveny CA et al. (2009a) Ah receptor represses acutephase response gene expression without binding to its cognate response element. Lab Invest 89:695-707
40. Patel RD, Murray IA, Flaveny CA et al. (2009b) Ah receptor represses acutephase response gene expression without binding to its cognate response element. Lab Invest 89:695-707
41. Poland A, Knutson JC (1982) 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: examination of the mechanism of toxicity. Annu Rev Pharmacol Toxicol 22:517-54
42. Qiu J, Heller JJ, Guo X et al. (2012) The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36:92-104
43. Reiners JJ Jr., Cantu AR, Pavone A (1990) Modulation of constitutive cytochrome P-450 expression in vivo and in vitro in murine keratinocytes as a function of differentiation and extracellular Ca2+ concentration. Proc Natl Acad Sci US A 87:1825-9
44. Reiners JJ Jr., Cantu AR, Thai G et al. (1992) Differential expression of basal and hydrocarbon-induced cytochrome P-450 monooxygenase and quinone reductase activities in subpopulations of murine epidermal cells differing in their stages of differentiation. Drug Metab Dispos 20:360-6
45. Rheinwald JG, Green H (1975) Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinising colonies from single cells. Cell 6:331-44
46. Robertson ED, Weir L, Romanowska M et al. (2012) ARNT controls the expression of epidermal differentiation genes through. J Cell Sci 125:3320-32
47. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-86
48. Sadek CM, len-Hoffmann BL (1994) Cytochrome P450IA1 is rapidly induced in normal human keratinocytes in the absence of xenobiotics. J Biol Chem 269:16067-74
49. Schmidt JV, Su GH, Reddy JK et al. (1996) Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci USA 93:6731-6
50. Schroeder JC, DiNatale BC, Murray IA et al. (2010) The uremic toxin 3-indoxyl sulfate is a potent endogenous agonist for the human aryl hydrocarbon receptor. Biochemistry 49:393-400
51. Seidel SD, Winters GM, Rogers WJ et al. (2001) Activation of the Ah receptor signaling pathway by prostaglandins. J Biochem Mol Toxicol 15:187-96
52. Shigeno T, Katakuse M, Fujita T et al. (2009) Phthalate ester-induced thymic stromal lymphopoietin mediates allergic dermatitis in mice. Immunology 128:e849-57
53. Shimizu Y, Nakatsuru Y, Ichinose M et al. (2000) Benzo[a]pyrene carcinogenicity is lost in mice lacking the aryl hydrocarbon receptor. Proc Natl Acad Sci USA 97:779-82
54. Smith KJ, Murray IA, Tanos R et al. (2011) Identification of a high-affinity ligand that exhibits complete aryl hydrocarbon receptor antagonism. J Pharmacol Exp Ther 338:318-27
55. Sutter CH, Bodreddigari S, Campion C et al. (2011) 2, 3, 7, 8-Tetrachlorodibenzo- p-dioxin increases the expression of genes in the human epidermal differentiation complex and accelerates epidermal barrier formation. Toxicol Sci 124:128-37
56. Sutter CH, Yin H, Li Y et al. (2009) EGF receptor signaling blocks aryl hydrocarbon receptor-mediated transcription and cell differentiation in human epidermal keratinocytes. Proc Natl Acad Sci USA 106:4266-71
57. Swanson HI (2004) Cytochrome P450 expression in human keratinocytes: an aryl hydrocarbon receptor perspective. Chem Biol Interact 149:69-79
58. Takemoto H, Tamai K, Akasaka E et al. (2010) Relation between the expression levels of the POU transcription factors Skn-1a and Skn-1n and keratinocyte differentiation. J Dermatol Sci 60:203-5
59. Tanos R, Patel RD, Murray IA et al. (2012) Aryl hydrocarbon receptor regulates the cholesterol biosynthetic pathway in a dioxin response elementindependent manner. Hepatology 55:1994-2004
60. Tortola L, Rosenwald E, Abel B et al. (2012) Psoriasiform dermatitis is driven by IL-36-mediated DC-keratinocyte crosstalk. J Clin Invest 122:3965-76
61. Van den Bogaard EH, Bergboer JG, Vonk-Bergers M et al. (2013) Coal tar induces AHR-dependent skin barrier repair in atopic dermatitis. J Clin Invest 123:917-27
62. Van den Bogaard EH, Rodijk-Olthuis D, Jansen PA et al. (2012) Rho kinase inhibitor Y-27632 prolongs the life span of adult human keratinocytes, enhances skin equivalent development, and facilitates lentiviral transduction. Tissue Eng Part A 18:1827-36
63. Van Ruissen F, de Jongh GJ, Zeeuwen PL et al. (1996) Induction of normal and psoriatic phenotypes in submerged keratinocyte cultures. J Cell Physiol 168:442-52
64. Veldhoen M, Hirota K, Christensen J et al. (2009) Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 T cells. J Exp Med 206:43-9
65. Wanner R, Brommer S, Czarnetzki BM et al. (1995) The differentiation-related upregulation of aryl hydrocarbon receptor transcript levels is suppressed by retinoic acid. Biochem Biophys Res Commun 209:706-11
66. Wincent E, Bengtsson J, Mohammadi BA et al. (2012) Inhibition of cytochrome P4501-dependent clearance of the endogenous agonist FICZ as a mechanism for activation of the aryl hydrocarbon receptor. Proc Natl Acad Sci USA 109:4479-84
67. Xu Y, Yang L, Yang T et al. (2008) Expression pattern of cyclooxygenase-2 in normal rat epidermis and pilosebaceous unit during hair cycle. Acta Histochem Cytochem 41:157-63