The tryptophan-derived endogenous aryl hydrocarbon receptor ligand 6-formylindolo[3,2-b]carbazole is a nanomolar UVA photosensitizer in epidermal keratinocytes

Journal of Investigative Dermatology

Volumn 135, Issue 6, 2015, Pages 1649-1658

  Park, Sophia L ^a   Justiniano, Rebecca ^a   Williams, Joshua D ^a   Cabello, Christopher M ^a   Qiao, Shuxi ^a   Wondrak, Georg T ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CARBAZOLE DERIVATIVE; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; PHOTOSENSITIZING AGENT; TRYPTOPHAN; 6-FORMYLINDOLO(3,2-B)CARBAZOLE; ANTIOXIDANT; DNA; DNA GLYCOSYLTRANSFERASE; LIGAND;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; EPIDERMIS CELL; GENE EXPRESSION; HEAT SHOCK; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KERATINOCYTE; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PHOTODYNAMICS; PHOTOSENSITIZATION; PHOTOTOXICITY; PRIORITY JOURNAL; SOLAR ENERGY; ULTRAVIOLET A RADIATION; ANIMAL; CELL LINE; CHEMISTRY; DRUG EFFECTS; EPIDERMIS; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; METABOLISM; PHOTOCHEMOTHERAPY; POLYMERASE CHAIN REACTION; PROCEDURES; RADIATION RESPONSE; SKIN;

ANIMALS; ANTIOXIDANTS; CARBAZOLES; CELL LINE; DNA; DNA GLYCOSYLASES; EPIDERMIS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; LIGANDS; MICE; OXIDATIVE STRESS; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; POLYMERASE CHAIN REACTION; RECEPTORS, ARYL HYDROCARBON; SKIN; TRYPTOPHAN;

EID: 84947048115     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.503     Document Type: Article

References (39)

1. Agar NS, Halliday GM, Barnetson RS et al. (2004) The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis. Proc Natl Acad Sci USA 101:4954-9
2. Agostinis P, Garmyn M, Van Laethem A (2007) The Aryl hydrocarbon receptor: an illuminating effector of the UVB response. Sci STKE 403:pe49
3. Andley UP, Clark BA (1989) Generation of oxidants in the near-UV photo-oxidation of human lens alpha-crystallin. Invest Ophthalmol Vis Sci 30:706-13
4. Baier J, Maisch T, Maier M et al. (2006) Singlet oxygen generation by UVA light exposure of endogenous photosensitizers. Biophys J 91:1452-9
5. Cadet J, Douki T, Ravanat JL et al. (2009) Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation. Photochem Photobiol Sci 8:903-11
6. Esser C, Bargen I, Weighardt H et al. (2013) Functions of the aryl hydrocarbon receptor in the skin. Semin Immunopathol 35:677-91
7. Fritsche E, Schafer C, Calles C et al. (2007) Lightening up the UV response by identification of the aryl hydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation. Proc Natl Acad Sci USA 104:8851-6
8. Gaitanis G, Magiatis P, Hantschke M et al. (2012) The Malassezia genus in skin and systemic diseases. Clin Microbiol Rev 25:106-41
9. Haarmann-Stemmann T, Abel J, Fritsche E et al. (2012) The AhR-Nrf2 pathway in keratinocytes: on the road to chemoprevention? J Invest Dermatol 132:7-9
10. Katiyar SK, Matsui MS, Mukhtar H (2000) Ultraviolet-B exposure of human skin induces cytochromes P450 1A1 and 1B1. J Invest Dermatol 114: 328-33
11. Kennedy JC, Pottier RH (1992) Endogenous protoporphyrin IX, a clinically useful photosensitizer for photodynamic therapy. J Photochem Photobiol B 14:275-92
12. Kipp C, Young AR (1999) The soluble eumelanin precursor 5, 6-dihydroxyin-dole-2-carboxylic acid enhances oxidative damage in human keratinocyte DNA after UVA irradiation. Photochem Photobiol 70:191-8
13. Lamore SD, Azimian S, Horn D et al. (2010a) The malondialdehyde-derived fluorophore DHP-lysine is a potent sensitizer of UVA-induced photooxidative stress in human skin cells. J Photochem Photobiol B 101:251-64
14. Lamore SD, Cabello CM, Wondrak GT (2010b) The topical antimicrobial zinc pyrithione is a heat shock response inducer that causes DNA damage and PARP-dependent energy crisis in human skin cells. Cell Stress Chaperones 15:309-22
15. Lamore SD, Qiao S, Horn D et al. (2010c) Proteomic identification of cathepsin B and nucleophosmin as novel UVA-targets in human skin fibroblasts. Photochem Photobiol 86:1307-17
16. Lamore SD, Wondrak GT (2011) Zinc pyrithione impairs zinc homeostasis and upregulates stress response gene expression in reconstructed human epidermis. Biometals 24:875-90
17. Luecke S, Backlund M, Jux B et al. (2010) The aryl hydrocarbon receptor (AHR), a novel regulator of human melanogenesis. Pigment Cell Melanoma Res 23:828-33
18. Magiatis P, Pappas P, Gaitanis G et al. (2013) Malassezia yeasts produce a collection of exceptionally potent activators of the Ah (dioxin) receptor detected in diseased human skin. J Invest Dermatol 133:2023-30
19. Marionnet C, Pierrard C, Lejeune F et al. (2010) Different oxidative stress response in keratinocytes and fibroblasts of reconstructed skin exposed to non extreme daily-ultraviolet radiation. PLoS One 5:e12059
20. Menon EL, Morrison H (2002) Formation of singlet oxygen by urocanic acid by UVA irradiation and some consequences thereof. Photochem Photobiol 75:565-9
21. Mukai M, Tischkau SA (2007) Effects of tryptophan photoproducts in the circadian timing system: searching for a physiological role for aryl hydrocarbon receptor. Toxicol Sci 95:172-81
22. Oberg M, Bergander L, Hakansson H et al. (2005) Identification of the tryptophan photoproduct 6-formylindolo[3, 2-b]carbazole, in cell culture medium, as a factor that controls the background aryl hydrocarbon receptor activity. Toxicol Sci 85:935-43
23. Qiao S, Tao S, Rojo de la Vega M et al. (2013) The antimalarial amodiaquine causes autophagic-lysosomal and proliferative blockade sensitizing human melanoma cells to starvation-and chemotherapy-induced cell death. Autophagy 9:2087-102
24. Quintana FJ, Basso AS, Iglesias AH et al. (2008) Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453: 65-71
25. Rannug A, Fritsche E (2006) The aryl hydrocarbon receptor and light. Biol Chem 387:1149-57
26. Sato K, Taguchi H, Maeda T et al. (1995) The primary cytotoxicity in ultraviolet-a-irradiated riboflavin solution is derived from hydrogen peroxide. J Invest Dermatol 105:608-12
27. Scharffetter-Kochanek K, Wlaschek M, Brenneisen P et al. (1997) UV-induced reactive oxygen species in photocarcinogenesis and photoaging. Biol Chem 378:1247-57
28. Tigges J, Haarmann-Stemmann T, Vogel CF et al. (2014) The new aryl hydrocarbon receptor antagonist E/Z-2-benzylindene-5, 6-dimethoxy-3, 3-dimethylindan-1-one protects against UVB-induced signal transduction. J Invest Dermatol 134:556-9
29. Wei YD, Rannug U, Rannug A (1999) UV-induced CYP1A1 gene expression in human cells is mediated by tryptophan. Chem Biol Interact 118: 127-40
30. Williams JD, Bermudez Y, Park SL et al. (2014) Malondialdehyde-derived epitopes in human skin result from acute exposure to solar UV and occur in nonmelanoma skin cancer tissue. J Photochem Photobiol B 132:56-65
31. Wincent E, Amini N, Luecke S et al. (2009) The suggested physiologic aryl hydrocarbon receptor activator and cytochrome P4501 substrate 6-formy-lindolo[3, 2-b]carbazole is present in humans. J Biol Chem 284:2690-6
32. Wincent E, Bengtsson J, Mohammadi Bardbori A 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
33. Wondrak GT, Cabello CM, Villeneuve NF et al. (2008) Cinnamoyl-based Nrf2-activators targeting human skin cell photo-oxidative stress. Free Radic Biol Med 45:385-95
34. Wondrak GT, Jacobson EL, Jacobson MK (2002) Photosensitization of DNA damage by glycated proteins. Photochem Photobiol Sci 1:355-63
35. Wondrak GT, Jacobson MK, Jacobson EL (2006) Endogenous UVA-photo-sensitizers: mediators of skin photodamage and novel targets for skin photoprotection. Photochem Photobiol Sci 5:215-37
36. Wondrak GT, Roberts MJ, Cervantes-Laurean D et al. (2003) Proteins of the extracellular matrix are sensitizers of photo-oxidative stress in human skin cells. J Invest Dermatol 121:578-86
37. Wondrak GT, Roberts MJ, Jacobson MK et al. (2004) 3-Hydroxypyridine chromophores are endogenous sensitizers of photooxidative stress in human skin cells. J Biol Chem 279:30009-20
38. Wright A, Hawkins CL, Davies MJ (2003) Photo-oxidation of cells generates long-lived intracellular protein peroxides. Free Radic Biol Med 34:637-47
39. Zastrow L, Groth N, Klein F et al. (2009) The missing link-light-induced (280-1, 600 nm) free radical formation in human skin. Skin Pharmacol Physiol 22:31-44