Phase II enzyme inducer, sulforaphane, inhibits UVB-induced AP-1 activation in human keratinocytes by a novel mechanism

Molecular Carcinogenesis

Volumn 41, Issue 3, 2004, Pages 179-186

  Zhu, Ming ^a   Zhang, Yuesheng ^b   Cooper, Simon ^a   Sikorski, Ewa ^a   Rohwer, John ^a   Bowden, G Timothy ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

AP 1; HaCaT; Phase II enzymes; Sulforaphane; UVB

Indexed keywords

GLUTATHIONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SULFORAPHANE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INCUBATION TIME; KERATINOCYTE; PLASMID; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN INDUCTION; REPORTER GENE; TRANSCRIPTION INITIATION; ULTRAVIOLET B RADIATION;

ANTICARCINOGENIC AGENTS; BINDING SITES; CALCIUM-TRANSPORTING ATPASES; CELLS, CULTURED; COLLAGENASES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME ACTIVATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GLUTATHIONE; HUMANS; HYDROQUINONES; KERATINOCYTES; LUCIFERASES; NAD(P)H DEHYDROGENASE (QUINONE); PROMOTER REGIONS (GENETICS); THIOCYANATES; TRANSCRIPTION FACTOR AP-1; TRANSFECTION; ULTRAVIOLET RAYS;

EID: 7244258809     PISSN: 08991987     EISSN: None     Source Type: Journal    
DOI: 10.1002/mc.20052     Document Type: Article

References (46)

1. Jemal A, Thomas A, Murray T, Thun M. Cancer statistics, 2002. CA Cancer J Clin 2002;52:23-47.
2. Ananthaswamy HN, Pierceall WE. Molecular mechanisms of ultraviolet radiation carcinogenesis. Photochem Photobiol 1990;52:1119-1136.
3. Barthelman M, Chen W, Gensler HL, Huang C, Dong Z, Bowden GT. Inhibitory effects of perillyl alcohol on UVB-induced murine skin cancer and AP-1 transactivation. Cancer Res 1998;58:711-716.
4. Huang C, Ma WY, Hanenberger D, Cleary MP, Bowden GT, Dong Z. Inhibition of ultraviolet B-induced activator protein-1 (AP-1) activity by aspirin in AP-1-luciferase transgenic mice. J Biol Chem 1997;272:26325-26331.
5. Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol 2002;4:E131-E136.
6. Young MR, Li JJ, Rincon M, et al. Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion. Proc Natl Acad Sci USA 1999;96:9827-9832.
7. Watts RG, Ben-Ari ET, Bernstein LR, et al. c-Jun and multistage carcinogenesis: Association of overexpression of introduced c-jun with progression toward a neoplastic endpoint in mouse JB6 cells sensitive to tumor promoter-induced transformation. Mol Carcinog 1995;13:27-36.
8. Li JJ, Rhim JS, Schlegel R, Vousden KH, Colburn NH. Expression of dominant negative Jun inhibits elevated AP-1 and NF-kappaB transactivation and suppresses anchorage independent growth of HPV immortalized human keratinocytes. Oncogene 1998;16:2711-2721.
9. Huang C, Ma WY, Dawson MI, Rincon M, Flavell RA, Dong Z. Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid. Proc Natl Acad Sci USA 1997;94:5826-5830.
10. Cooper SJ, MacGowan J, Ranger-Moore J, Young MR, Colburn NH, Bowden GT. Expression of dominant negative c-jun inhibits ultraviolet B-induced squamous cell carcinoma number and size in an SKH-1 hairless mouse model. Mol Cancer Res 2003;1:848-854.
11. Garmyn M, Degreef H. Suppression of UVB-induced c-fos and c-jun expression in human keratinocytes by N-acetylcysteine. J Photochem Photobiol B 1997;37:125-130.
12. Kramer-Stickland K, Edmonds A, Bair WB, Bowden GT. Inhibitory effects of deferoxamine on UVB-induced AP-1 transactivation. Carcinogenesis 1999;20:2137-2142.
13. Ding M, Li JJ, Leonard SS, et al. Vanadate-induced activation of activator protein-1: Role of reactive oxygen species. Carcinogenesis 1999;20:663-668.
14. Amstad PA, Krupitza G, Cerutti PA. Mechanism of c-fos induction by active oxygen. Cancer Res 1992;52:3952-3960.
15. Peus D, Vasa RA, Beyerle A, Meves A, Krautmacher C, Pittelkow MR. UVB activates ERK1/2 and p38 signaling pathways via reactive oxygen species in cultured keratinocytes. J Invest Dermatol 1999;112:751-756.
16. Talalay P, Dinkova-Kostova AT, Holtzclaw WD. Importance of phase II gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Adv Enzyme Regulat 2003;43:121-134.
17. Hayes JD, McLellan LI. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 1999;31:273-300.
18. Fahey JW, Talalay P. Antioxidant functions of sulforaphane: A potent inducer of Phase II detoxication enzymes. Food Chem Toxicol 1999;37:973-979.
19. Wattenberg LW, Coccia JB, Lam LK. Inhibitory effects of phenolic compounds on benzo(a)pyrene-induced neoplasia. Cancer Res 1980;40:2820-2823.
20. Zhang Y, Talalay P, Cho CG, Posner GH. A major inducer of anticarcinogenic protective enzymes from broccoli: Isolation and elucidation of structure. Proc Natl Acad Sci USA 1992;89:2399-2403.
21. Mahéo K, Morel F, Langouët S, et al. Inhibition of cytochromes P-450 and induction of glutathione S-transferases by sulforaphane in primary human and rat hepatocytes. Cancer Res 1997;57:3649-3652.
22. Lee SK, Song L, Mata-Greenwood E, Kelloff GJ, Steele VE, Pezzuto JM. Modulation of in vitro biomarkers of the carcinogenic process by chemopreventive agents. Anticancer Res 1999;19:35-44.
23. Gamet-Payrastre L, Li P, Lumeau S, et al. Sulforaphane, a naturally occurring isothiocyanate, induces cell-cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res 2000;60:1426-1433.
24. Heiss E, Herhaus C, Klimo K, Bartsch H, Gerhäuser C. Nuclear factor B is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms. J Biol Chem 2001;276:32008-32015.
25. Rehwoldt R. Tracking the use of antioxidants through industry surveys. Food Chem Toxicol 1986;24:1039-1041.
26. Zhang Y, Gonzalez V, Xu MJ. Expression and regulation of glutathione S-transferase P1-1 in cultured human epidermal cells. J Dermatol Sci 2002;30:205-214.
27. Anderson ME. Glutathione: An overview of biosynthesis and modulation. Chem Biol Interact 1998;111-112:1-14.
28. Talalay P. Chemoprotection against cancer by induction of phase 2 enzymes. Biofactors 2000;12:5-11.
29. Chen W, Borchers AH, Dong Z, Powell MB, Bowden GT. UVB irradiation-induced activator protein-1 activation correlates with increased c-fos gene expression in a human keratinocyte cell line. J Biol Chem 1998;273:32176-32181.
30. Gonzales M, Bowden GT. Nordihydroguaiaretic acid-mediated inhibition of ultraviolet B-induced activator protein-1 activation in human keratinocytes. Mol Carcinog 2002;34:102-111.
31. Chen W, Bowden GT. Role of p38 mitogen-activated protein kinases in ultraviolet-B irradiation-induced activator protein 1 activation in human keratinocytes. Mol Carcinog 2000;28196-28202.
32. Posner GH, Cho CG, Green JV, Zhang Y, Talalay P. Design and synthesis of bifunctional isothiocyanate analogs of sulforaphane: Correlation between structure and potency as inducers of anticarcinogenic detoxication enzymes. J Med Chem 1994;7:170-176.
33. Richie JP Jr., Skowronski L, Abraham P, Leutzinger Y. Blood glutathione concentrations in a large-scale human study. Clin Chem 1996;42:64-70.
34. Gerhauser C, You M, Liu J, et al. Cancer chemopreventive potential of sulforamate, a novel analogue of sulforaphane that induces phase 2 drug-metabolizing enzymes. Cancer Res 1997;57:272-278.
35. Zhang Y. Molecular mechanism of rapid cellular accumulation of anticarcinogenic isothiocyanates. Carcinogenesis 2001;22:425-431.
36. Zhang Y. Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis 2000;21:1175-1182.
37. Heck DE, Vetrano AM, Mariano TM, Laskin JD. UVB light stimulates production of reactive oxygen species: Unexpected role for catalase. J Biol Chem 2003;278:22432-22436.
38. Soriani M, Hejmadi V, Tyrrell RM. Modulation of c-jun and c-fos transcription by UVB and UVA radiations in human dermal fibroblasts and KB cells. Photochem Photobiol 2000;71:551-558.
39. Isoherranen K, Westermarck J, Kahari VM, Jansen C, Punnonen K. Differential regulation of the AP-1 family members by UV irradiation in vitro and in vivo. Cell Signal 1998;10:191-195.
40. Grandjean-Laquerriere A, Gangloff SC, Le Naour R, Trentesaux C, Hornebeck W, Guenounou M. Relative contribution of NF-kappaB and AP-1 in the modulation by curcumin and pyrrolidine dithiocarbamate of the UVB-induced cytokine expression by keratinocytes. Cytokine 2002;18:168-177.
41. Abate C, Patel L, Rauscher FJ, Curran T. Redox regulation of fos and jun DNA-binding activity in vitro. Science 1990;249:1157-1161.
42. Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, Hay RT. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 1992;20:3821-3830.
43. Xanthoudakis S, Curran T. Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J 1992;11:653-665.
44. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, et al. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci USA 2002;99:11908-11913.
45. Gills JJ, Jeffery EH, Moon RC, Lantvit DD, Pezzuto JM. Effects of sulphoraphane on UVB-induced skin carcinogenesis. Proceedings of American Association for Cancer Research (94th Annual Meeting). 2003;44:223.
46. Ostrowski J, Woszczynski M, Kowalczyk P, et al. Increased activity of MAP, p70S6, and p90rs kinases is associated with AP-1 activation in spontaneous liver tumours, but not in adjacent tissue in mice. Br J Cancer 2000;82:1041-1050.