Apigenin reactivates Nrf2 anti-oxidative stress signaling in mouse skin epidermal JB6 P + cells through epigenetics modifications

AAPS Journal

Volumn 16, Issue 4, 2014, Pages 727-735

  Paredes Gonzalez, Ximena ^a   Fuentes, Francisco ^a   Su, Zheng Yuan ^a   Kong, Ah Ng Tony ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

apigenin; DNMTs; epigenetics; HDACs; Nrf2; skin cancer

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANTIBODY; APIGENIN; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 8; MESSENGER RNA; METHYLCYTOSINE ANTIBODY; TRANSCRIPTION FACTOR NRF2; TRICHOSTATIN A; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; HDAC1 PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; PROTEIN SYNTHESIS INHIBITOR;

ANIMAL CELL; ANTIGEN BINDING; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CANCER PREVENTION; CHEMOPROPHYLAXIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; DNA SEQUENCE; DRUG CYTOTOXICITY; DRUG EFFICACY; ENZYME INHIBITION; EPIDERMIS CELL; EPIGENETICS; GENE EXPRESSION; GENE TRANSLOCATION; IN VITRO STUDY; MOUSE; NONHUMAN; NQO1 GENE; NRF2 GENE; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN CANCER; ANIMAL; BIOSYNTHESIS; CELL LINE; CYTOLOGY; DRUG EFFECTS; EPIDERMIS; GENETIC EPIGENESIS; GENETICS; METABOLIC ACTIVATION; METABOLISM;

ACTIVATION, METABOLIC; ANIMALS; APIGENIN; CELL LINE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIDERMIS; EPIGENESIS, GENETIC; HISTONE DEACETYLASE 1; MICE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEIN SYNTHESIS INHIBITORS; SIGNAL TRANSDUCTION;

EID: 84903640329     PISSN: None     EISSN: 15507416     Source Type: Journal    
DOI: 10.1208/s12248-014-9613-8     Document Type: Article

References (46)

1. Lomas A, Leonardi-Bee J, Bath-Hextall F. A systematic review of worldwide incidence of nonmelanoma skin cancer. Br J Dermatol. 2012;166(5):1069-80.
2. Lewis KG, Weinstock MA. Trends in nonmelanoma skin cancer mortality rates in the United States, 1969 through 2000. J Invest Dermatol. 2007;127(10):2323-7. (Pubitemid 47619763)
3. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: A Cancer J Clin. 2014;64(1):9-29.
4. Halliday GM, Byrne SN, Damian DL. Ultraviolet A radiation: its role in immunosuppression and carcinogenesis. Semin Cutan Med Surg. 2011;30(4):214-21.
5. Hussein MR. Ultraviolet radiation and skin cancer: molecular mechanisms. J Cutan Pathol. 2005;32(3):191-205. (Pubitemid 40278816)
6. Nandakumar V, Vaid M, Tollefsbol TO, Katiyar SK. Aberrant DNA hypermethylation patterns lead to transcriptional silencing of tumor suppressor genes in UVB-exposed skin and UVBinduced skin tumors of mice. Carcinogenesis. 2011;32(4):597- 604.
7. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002;3(6):415-28. (Pubitemid 34587077)
8. Sathyanarayana UG, Moore AY, Li L, Padar A, Majmudar K, Stastny V, et al. Sun exposure related methylation in malignant and non-malignant skin lesions. Cancer Lett. 2007;245(1-2):112-20. (Pubitemid 44959343)
9. Brown VL, Harwood CA, Crook T, Cronin JG, Kelsell DP, Proby CM. p16INK4a and p14ARF tumor suppressor genes are commonly inactivated in cutaneous squamous cell carcinoma 2004 [cited 122 5]. 1284-92]. Available from: :// MEDLINE:15140233.
10. van Doorn R, Zoutman WH, Dijkman R, de Menezes RX, Commandeur S, Mulder AA, et al. Epigenetic pro filing of cutaneous T-cell lymphoma: promoter hypermethylation of multiple tumor suppressor genes including BCL7a, PTPRG, and p73. J Clin Oncol. 2005;23(17):3886-96. (Pubitemid 46218691)
11. Lee JH, Khor TO, Shu L, Su Z-Y, Fuentes F, Kong A-NT. Dietary phytochemicals and cancer prevention: Nrf2 signaling, epigenetics, and cell death mechanisms in blocking cancer initiation and progression. Pharmacol Ther. 2013;137(2):153-71.
12. Su ZY, Zhang C, Lee JH, Shu L, Wu TY, Khor TO, et al. Requirement and epigenetics re-programming of Nrf2 in suppression of tumor promoter TPA-induced mouse skin cell transformation by sulforaphane. Cancer prevention research. 2014.
13. Su ZY, Shu L, Khor TO, Lee JH, Fuentes F, Kong AN. A perspective on dietary phytochemicals and cancer chemoprevention: oxidative stress, nrf2, and epigenomics. Top Curr Chem. 2013;329:133-62.
14. Yu S, Khor TO, Cheung K-L, Li W, Wu T-Y, Huang Y, et al. Nrf2 expression is regulated by epigenetic mechanisms in prostate cancer of TRAMP mice. PLoS One. 2010;5(1):e8579.
15. Hatzimichael E, Crook T. Cancer epigenetics: new therapies and new challenges. J Drug Deliv. 2013;2013:529312.
16. Katiyar SK, Singh T, Prasad R, Sun Q, Vaid M. Epigenetic alterations in ultraviolet radiation-induced skin carcinogenesis: interaction of bioactive dietary components on epigenetic targets. Photochem Photobiol. 2012;88(5):1066-74.
17. Baumann LS. Less-known botanical cosmeceuticals. Dermatol Ther. 2007;20(5):330-42. (Pubitemid 350197164)
18. Patel D, Shukla S, Gupta S. Apigenin and cancer chemoprevention: progress, potential and promise (review). Int J Oncol. 2007;30(1):233-45.
19. Shukla S, Gupta S. Apigenin: a promising molecule for cancer prevention. Pharm Res. 2010;27(6):962-78.
20. Merfort I, Heilmann J, Hagedorn-Leweke U, Lippold BC. In vivo skin penetration studies of camomile flavones. Pharmazie. 1994;49(7):509-11. (Pubitemid 24240336)
21. Li B, Birt DF. In vivo and in vitro percutaneous absorption of cancer preventive fl avonoid apigenin in different vehicles in mouse skin. Pharm Res. 1996;13(11):1710-5. (Pubitemid 26426897)
22. Li B, Pinch H, Birt DF. Influence of vehicle, distant topical delivery, and biotransformation on the chemopreventive activity of apigenin, a plant flavonoid, in mouse skin. Pharm Res. 1996;13(10):1530-4. (Pubitemid 26356957)
23. Wei H, Tye L, Bresnick E, Birt DF. Inhibitory effect of apigenin, a plant fl avonoid, on epidermal ornithine decarboxylase and skin tumor promotion in mice. Cancer Res. 1990;50(3):499-502. (Pubitemid 20054168)
24. Birt DF, Mitchell D, Gold B, Pour P, Pinch HC. Inhibition of ultraviolet light induced skin carcinogenesis in SKH-1 mice by apigenin, a plant flavonoid. Anticancer Res. 1997;17(1A):85-91. (Pubitemid 27116649)
25. Caltagirone S, Rossi C, Poggi A, Ranelletti FO, Natali PG, Brunetti M, et al. Flavonoids apigenin and quercetin inhibit melanoma growth and metastatic potential. Int J Cancer. 2000;87(4):595-600. (Pubitemid 30639822)
26. Fang M, Chen D, Yang CS. Dietary polyphenols may affect DNA methylation. J Nutr. 2007;137(1 Suppl):223S-8.
27. Pandey M, Kaur P, Shukla S, Abbas A, Fu P, Gupta S. Plant flavone apigenin inhibits HDAC and remodels chromatin to induce growth arrest and apoptosis in human prostate cancer cells: in vitro and in vivo study. Mol Carcinog. 2012;51(12):952-62.
28. Khor TO, Huang Y, Wu T-Y, Shu L, Lee J, Kong A-NT. Pharmacodynamics of curcumin as DNA hypomethylation agent in restoring the expression of Nrf2 via promoter CpGs demethylation. Biochem Pharmacol. 2011;82(9):1073-8.
29. Fuentes F, Shu L, Lee JH, Su Z-Y, Lee K-R, Kong A-NT. Nrf2- target approaches in cancer chemoprevention mediated by dietary phytochemicals. In: Bode AM, Dong Z, editors. Cancer prevention: methods in pharmacology and toxicology. New York: Springer; 2014. p. 53-83.
30. IchihashiM,UedaM,BudiyantoA, Bito T,OkaM, FukunagaM, et al. UV-induced skin damage. Toxicology. 2003;189(1-2):21-39.
31. Schafer M, Dutsch S, auf dem Keller U, Werner S. Nrf2: a central regulator of UV protection in the epidermis. Cell Cycle. 2010;9(15):2917-8.
32. Xu C, Huang M-T, Shen G, Yuan X, Lin W, Khor TO, 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(16):8293-6. (Pubitemid 44299200)
33. auf dem Keller U, Huber M, Beyer TA, Kumin A, Siemes C, Braun S, et al. Nrf transcription factors in keratinocytes are essential for skin tumor prevention but not for wound healing. Mol Cell Biol. 2006;26(10):3773-84. (Pubitemid 43726395)
34. Schafer M, Dutsch S, auf dem Keller U, Navid F, Schwarz A, Johnson DA. Nrf2 establishes a glutathione-mediated gradient of UVB cytoprotection in the epidermis. Genes Dev. 2010;24(10):1045-58.
35. Lepley DM, Pelling JC. Induction of p21/WAF1 and G1 cellcycle arrest by the chemopreventive agent apigenin. Mol Carcinog. 1997;19(2):74-82. (Pubitemid 27296738)
36. McVean M, Weinberg WC, Pelling JC. A p21(waf1)-independent pathway for inhibitory phosphorylation of cyclin-dependent kinase p34(cdc2) and concomitant G(2)/M arrest by the chemopreventive flavonoid apigenin. Mol Carcinog. 2002;33(1):36-43. (Pubitemid 34052305)
37. Tong X, Pelling JC. Enhancement of p53 expression in keratinocytes by the bioflavonoid apigenin is associated with RNA-binding protein HuR. Mol Carcinog. 2009;48(2):118-29.
38. Huang YT, Kuo ML, Liu JY, Huang SY, Lin JK. Inhibitions of protein kinase C and proto-oncogene expressions in NIH 3 T3 cells by apigenin. Eur J Cancer. 1996;32A(1):146-51.
39. Tong X, Van Dross RT, Abu-Yousif A, Morrison AR, Pelling JC. Apigenin prevents UVB-induced cyclooxygenase 2 expression: coupled mRNA stabilization and translational inhibition. Mol Cell Biol. 2007;27(1):283-96. (Pubitemid 46013251)
40. Van Dross RT, Hong X, Pelling JC. Inhibition of TPA-induced cyclooxygenase-2 (COX-2) expression by apigenin through downregulation of Akt signal transduction in human keratinocytes. Mol Carcinog. 2005;44(2):83-91. (Pubitemid 41397173)
41. Byun S, Park J, Lee E, Lim S, Yu JG, Lee SJ, et al. Src kinase is a direct target of apigenin against UVB-induced skin inflammation. Carcinogenesis. 2013;34(2):397-405.
42. Arango D, Morohashi K, Yilmaz A, Kuramochi K, Parihar A, Brahimaj B, et al. Molecular basis for the action of a dietary fl avonoid revealed by the comprehensive identification of apigenin human targets. Proc Natl Acad Sci U S A. 2013;110(24):E2153-62.
43. Lee WJ, Shim J-Y, Zhu BT. Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids. Mol Pharmacol. 2005;68(4):1018-30. (Pubitemid 41345793)
44. Rajnee Kanwal HS, and Sanjay Gupta. Abstract 3683: Plant fl avonoid apigenin preferentially binds with GC-rich DNA sequences and inhibits DNA methylation. AACR Proceedings of the 102nd Annual Meeting of the American Association for Cancer Research; Orlando, FL: Cancer Research April 15, 2011; Volume 71, Issue 8, Supplement 1; 2011.
45. Nguyen T, Kuo C, Nicholl MB, Sim MS, Turner RR, Morton DL, et al. Downregulation of microRNA-29c is associated with hypermethylation of tumor-related genes and disease outcome in cutaneous melanoma. Epigenetics: Off J DNA Methylation Soc. 2011;6(3):388-94.
46. Hadnagy A, Beaulieu R, Balicki D. Histone tail modifications and noncanonical functions of histones: perspectives in cancer epigenetics. Mol Cancer Ther. 2008;7(4):740-8. (Pubitemid 351551027)