Inhibition of activator protein-1 by sulforaphane involves interaction with cysteine in the cFos DNA-binding domain: Implications for chemoprevention of UVB-induced skin cancer

Cancer Research

Volumn 69, Issue 17, 2009, Pages 7103-7110

  Dickinson, Sally E ^a   Melton, Tania F ^a   Olson, Erik R ^a   Zhang, Jian ^a   Saboda, Kathylynn ^a   Bowden, G Timothy ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; CYSTEINE; DIAMIDE; DNA; LUCIFERASE; NUCLEAR PROTEIN; PROTEIN C FOS; RECOMBINANT PROTEIN; SULFORAPHANE; TRANSCRIPTION FACTOR AP 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DNA BINDING; DRUG INHIBITION; ENZYME ACTIVITY; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; IMMUNOPRECIPITATION; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; SKIN CANCER; ULTRAVIOLET B RADIATION;

ANIMALS; ANTICARCINOGENIC AGENTS; BINDING SITES; CARCINOMA, SQUAMOUS CELL; CYSTEINE; DISEASE MODELS, ANIMAL; FEMALE; MICE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; RECOMBINANT PROTEINS; SKIN NEOPLASMS; THIOCYANATES; TRANSCRIPTION FACTOR AP-1; ULTRAVIOLET RAYS;

EID: 70149093188     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-0770     Document Type: Article

References (46)

1. 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 (Pubitemid 29177163)
2. 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 (Pubitemid 37174456)
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 (Pubitemid 28099482)
4. Li JJ, Dong Z, Dawson MI, Colburn NH. Inhibition of tumor promoter-induced transformation by retinoids that transrepress AP-1 without transactivating retinoic acid response element. Cancer Res 1996;56:483-489 (Pubitemid 26048602)
5. Kramer-Stickland K, Edmonds A, Bair WB III, Bowden GT. Inhibitory effects of deferoxamine on UVB-induced AP-1 transactivation. Carcinogenesis 1999;20:2137-2142 (Pubitemid 29535316)
6. Bowden GT. Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat Rev Cancer 2004;4:23-35.
7. Abate C, Patel L, Rauscher FJ III, Curran T. Redox regulation of fos and jun DNA-binding activity in vitro. Science 1990;249:1157-1161 (Pubitemid 20337316)
8. 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
9. Conaway CC, Wang CX, Pittman B, et al. Phenethyl isothiocyanate and sulforaphane and their N-acetylcysteine conjugates inhibit malignant progression of lung adenomas induced by tobacco carcinogens in A/J mice. Cancer Res 2005;65:8548-8557 (Pubitemid 41330624)
10. Hu R, Khor TO, Shen G, et al. Cancer chemoprevention of intestinal polyposis in ApcMin/+ mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis 2006;27:2038-2046 (Pubitemid 44530579)
11. Dinkova-Kostova AT, Jenkins SN, Fahey JW, et al. Protection against UV-light-induced skin carcinogenesis in SKH-1 high-risk mice by sulforaphane-containing broccoli sprout extracts. Cancer Lett 2006;240:243-252
12. Xu C, Huang MT, Shen G, et al. Inhibition of 7,12-dimethylbenz(a) anthracene-induced skin tumorigenesis in C57BL/6 mice by sulforaphane is mediated by nuclear factor E2-related factor 2. Cancer Res 2006;66:8293-8296 (Pubitemid 44299200)
13. Gills JJ, Jeffery EH, Matusheski NV, Moon RC, Lantvit DD, Pezzuto JM. Sulforaphane prevents mouse skin tumorigenesis during the stage of promotion. Cancer Lett 2006;236:72-79
14. Hong F, Freeman ML, Liebler DC. Identification of sensor cysteines in human Keap1 modified by the cancer chemopreventive agent sulforaphane. Chem Res Toxicol 2005;18:1917-1926 (Pubitemid 43023050)
15. Zhang DD, Lo SC, Sun Z, Habib GM, Lieberman MW, Hannink M. Ubiquitination of Keap1, a BTB-Kelch substrate adaptor protein for Cul3, targets Keap1 for degradation by a proteasome-independent pathway. J Biol Chem 2005;280:30091-30099 (Pubitemid 41216185)
16. 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.
17. Kim BR, Hu R, Keum YS, et al. Effects of glutathione on antioxidant response element-mediated gene expression and apoptosis elicited by sulforaphane. Cancer Res 2003;63:7520-7525 (Pubitemid 37413497)
18. Zhu M, Zhang Y, Cooper S, Sikorski E, Rohwer J, Bowden GT. Phase II enzyme inducer, sulforaphane, inhibits UVB-induced AP-1 activation in human keratinocytes by a novel mechanism. Mol Carcinog 2004;41:179-186 (Pubitemid 39435114)
19. Bair WB III, Hart N, Einspahr J, et al. Inhibitory effects of sodium salicylate and acetylsalicylic acid on UVB-induced mouse skin carcinogenesis. Cancer Epidemiol Biomarkers Prev 2002;11:1645-1652 (Pubitemid 36020019)
20. Rincon M, Flavell RA. AP-1 transcriptional activity requires both T-cell receptor-mediated and co-stimulatory signals in primary T lymphocytes. EMBO J 1994;13:4370-4381 (Pubitemid 24295209)
21. Bachelor MA, Cooper SJ, Sikorski ET, Bowden GT. Inhibition of p38 mitogen-activated protein kinase and phosphatidylinositol 3-kinase decreases UVB-induced activator protein-1 and cyclooxygenase-2 in a SKH-1 hairless mouse model. Mol Cancer Res 2005;3:90-99
22. Schenk PM, Baumann S, Mattes R, Steinbiss HH. Improved high-level expression system for eukaryotic genes in Escherichia coli using T7 RNA polymerase and rare ArgtRNAs. Biotechniques 1995;19:196-8, 200.
23. Ferguson HA, Goodrich JA. Expression and purification of recombinant human c-Fos/c-Jun that is highly active in DNA binding and transcriptional activation in vitro. Nucleic Acids Res 2001;29:E98.
24. Fitzgerald M, Oshiro M, Holtan N, et al. Human pancreatic carcinoma cells activate maspin expression through loss of epigenetic control. Neoplasia 2003;5:427-436 (Pubitemid 37475651)
25. Angel P, Baumann I, Stein B, Delius H, Rahmsdorf HJ, Herrlich P. 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5′-flanking region. Mol Cell Biol 1987;7:2256-2266
26. Talalay P, Fahey JW, Healy ZR, et al. Sulforaphane mobilizes cellular defenses that protect skin against damage by UV radiation. Proc Natl Acad Sci U S A 2007;104:17500-17505 (Pubitemid 350219867)
27. Dinkova-Kostova AT, Fahey JW, Wade KL, et al. Induction of the phase 2 response in mouse and human skin by sulforaphane-containing broccoli sprout extracts. Cancer Epidemiol Biomarkers Prev 2007;16:847-851
28. Cornblatt BS, Ye L, Dinkova-Kostova AT, et al. Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast. Carcinogenesis 2007;28:1485-1490 (Pubitemid 47241798)
29. Hirota A, Kawachi Y, Itoh K, et al. Ultraviolet A irradiation induces NF-E2-related factor 2 activation in dermal fibroblasts: protective role in UVA-induced apoptosis. J Invest Dermatol 2005;124:825-832 (Pubitemid 40489511)
30. Durchdewald M, Beyer TA, Johnson DA, Johnson JA, Werner S, auf dem Keller U. Electrophilic chemicals but not UV irradiation or reactive oxygen species activate Nrf2 in keratinocytes in vitro and in vivo. J Invest Dermatol 2007;127:646-653 (Pubitemid 46271033)
31. Marrot L, Jones C, Perez P, Meunier JR. The significance of Nrf2 pathway in (photo)-oxidative stress response in melanocytes and keratinocytes of the human epidermis. Pigment Cell Melanoma Res 2008;21:79-88.
32. Hayes JD, McMahon M. The double-edged sword of Nrf2: subversion of redox homeostasis during the evolution of cancer. Mol Cell 2006;21:732-734 (Pubitemid 43376123)
33. 2 and Nrf2 pathways in protection against acute lung injury. Am J Respir Crit Care Med 2005;171:1260-1266
34. Braun S, Hanselmann C, Gassmann MG, et al. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Mol Cell Biol 2002;22:5492-5505 (Pubitemid 34755759)
35. Woo KJ, Kwon TK. Sulforaphane suppresses lipopolysaccharide-induced cyclooxygenase-2 (COX-2) expression through the modulation of multiple targets in COX-2 gene promoter. Int Immunopharmacol 2007;7:1776-1783
36. Lin W, Wu RT, Wu T, Khor TO, Wang H, Kong AN. Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochem Pharmacol 2008;76:967-973
37. Cheung KL, Khor TO, Kong AN. Synergistic effect of combination of phenethyl isothiocyanate and sulforaphane or curcumin and sulforaphane in the inhibition of inflammation. Pharm Res 2009;26:224-231
38. Kawachi Y, Xu X, Taguchi S, et al. Attenuation of UVB-induced sunburn reaction and oxidative DNA damage with no alterations in UVB-induced skin carcinogenesis in Nrf2 gene-deficient mice. J Invest Dermatol 2008;128:1773-1779 (Pubitemid 351847374)
39. Jeong WS, Kim IW, Hu R, Kong AN. Modulation of AP-1 by natural chemopreventive compounds in human colon HT-29 cancer cell line. Pharm Res 2004;21:649-660 (Pubitemid 38457288)
40. Zhang Y. Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis 2000;21:1175-1182 (Pubitemid 30389344)
41. Okuno H, Akahori A, Sato H, Xanthoudakis S, Curran T, Iba H. Escape from redox regulation enhances the transforming activity of Fos. Oncogene 1993;8:695-701. (Pubitemid 23093133)
42. Chida K, Vogt PK. Nuclear translocation of viral Jun but not of cellular Jun is cell cycle dependent. Proc Natl Acad Sci U S A 1992;89:4290-4294
43. Maki Y, Bos TJ, Davis C, Starbuck M, Vogt PK. Avian sarcoma virus 17 carries the jun oncogene. Proc Natl Acad Sci U S A 1987;84:2848-2852
44. Shapiro TA, Fahey JW, Dinkova-Kostova AT, et al. Safety, tolerance, and metabolism of broccoli sprout glucosinolates and isothiocyanates: a clinical phase I study. Nutr Cancer 2006;55:53-62.
45. Kensler TW, Chen JG, Egner PA, et al. Effects of glucosinolate-rich broccoli sprouts on urinary levels of aflatoxin-DNA adducts and phenanthrene tetraols in a randomized clinical trial in He Zuo township, Qidong, People's Republic of China. Cancer Epidemiol Biomarkers Prev 2005;14:2605-2613
46. Heiss E, Herhaus C, Klimo K, Bartsch H, Gerhauser C. Nuclear factor κB is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms. J Biol Chem 2001;276:32008-32015 (Pubitemid 37384858)