Nrf2-target approaches in cancer chemoprevention mediated by dietary phytochemicals

Methods in Pharmacology and Toxicology

Volumn , Issue , 2014, Pages 53-83

  Fuentes, Francisco ^a,b   Shu, Limin ^a   Lee, Jong Hun ^a   Su, Zheng Yuan ^a   Lee, Kyeong Ryoon ^a   Kong, Ah Ng Tony ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSIDAD ARTURO PRAT   (Chile)

Author keywords

Cancer chemoprevention; Epigenetics; Nrf2; Nrf2 deficient mouse models; Pharmacodynamics; Pharmacokinetics

Indexed keywords

4 O METHYLPHORBOL 13 ACETATE 12 MYRISTATE; BISULFITE; DEXTRAN SULFATE; DIMETHYLBENZ[A]ANTHRACENE; DNA; DNA FRAGMENT; LUCIFERASE; PLANT MEDICINAL PRODUCT; REAGENT; TRANSCRIPTION FACTOR NRF2;

ANALYTICAL EQUIPMENT; ARTICLE; CELL ADHESION; CELL ASSAY; CELL STRAIN HEPG2; CHEMOPROPHYLAXIS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CROSS LINKING; DNA PURIFICATION; ENZYME ACTIVITY; EXPERIMENTAL ANIMAL; EXPERIMENTAL COLITIS; EXPERIMENTAL MODEL; GENE SEQUENCE; GENOME ANALYSIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MOLECULAR CLONING; NONHUMAN; PHARMACODYNAMICS; PHYTOCHEMISTRY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; REACTION ANALYSIS; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS;

EID: 84891774343     PISSN: 15572153     EISSN: 19406053     Source Type: Book Series    
DOI: 10.1007/978-1-4614-9227-6_3     Document Type: Article

References (67)

1. Wattenberg LW (1985) Chemoprevention of cancer. Cancer Res 45(1):1-8
2. Su ZY, Shu L, Khor TO, Lee JH, Fuentes F, Kong AN (2013) A perspective on dietary phytochemicals and cancer chemoprevention: oxidative stress, Nrf2, and epigenomics. Top Curr Chem 329:133-162. doi:10.1007/128-2012-340
3. Chen C, Pung D, Leong V, Hebbar V, Shen G, Nair S, Li W, Kong AN (2004) Induction of detoxifying enzymes by garlic organosulfur compounds through transcription factor Nrf2: effect of chemical structure and stress signals. Free Radic Biol Med 37(10):1578-1590. doi:10.1016/j.freeradbiomed.2004.07.021, pii:S0891-5849(04)00580-5
4. Yu S, Kong AN (2007) Targeting carcinogen metabolism by dietary cancer preventive compounds. Curr Cancer Drug Targets 7(5):416-424
5. He CH, Gong P, Hu B, Stewart D, Choi ME, Choi AM, Alam J (2001) Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J Biol Chem 276(24):20858-20865. doi:10.1074/jbc.M101198200M101198200
6. Jaiswal AK (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36(10):1199-1207. doi:10.1016/j. freeradbiomed, pii: 2004.02.074S0891584904001923
7. Levy S, Forman HJ (2010) C-Myc is a Nrf2-interacting protein that negatively regulates phase II genes through their electrophile responsive elements. IUBMB Life 62(3): 237-246. doi:10.1002/iub.314
8. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL (1999) Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274(37): 26071-26078
9. Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 275(21):16023-16029. doi:275/21/16023
10. Wu TY, Saw CL, Khor TO, Pung D, Boyanapalli SS, Kong AN (2012) In vivo pharmacodynamics of indole-3-carbinol in the inhibition of prostate cancer in transgenic adenocarcinoma of mouse prostate (TRAMP) mice: involvement of Nrf2 and cell cycle/apoptosis signaling pathways. Mol Carcinog 51(10):761-770. doi:10.1002/mc.20841
11. Sun Z, Wu T, Zhao F, Lau A, Birch CM, Zhang DD (2011) KPNA6 (Importin {alpha}7)-mediated nuclear import of Keap1 represses the Nrf2-dependent antioxidant response. Mol Cell Biol 31(9):1800-1811. doi:10.1128/MCB.05036-11, MCB.05036-11
12. Lee JH, Khor TO, Shu L, Su ZY, Fuentes F, Kong AN (2013) Dietary phytochemicals and cancer prevention: Nrf2 signaling, epigenetics, and cell death mechanisms in blocking cancer initiation and progression. Pharmacol Ther 137(2):153-171. doi:10.1016/j.pharmthera. 2012.09.008
13. Khor TO, Huang Y, Wu TY, Shu L, Lee J, Kong AN (2011) Pharmacodynamics of curcumin as DNA hypomethylation agent in restoring the expression of Nrf2 via promoter CpGs demethylation. Biochem Pharmacol 82(9):1073-1078. doi:10.1016/j.bcp.2011.07.065
14. Xu C, Huang MT, Shen G, Yuan X, Lin W, Khor TO, Conney AH, Kong AN (2006) 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 66(16):8293-8296. doi:10.1158/0008-5472.CAN-06-0300
15. Zhang C, Su ZY, Khor TO, Shu L, Kong AN (2013) Sulforaphane enhances Nrf2 expression in prostate cancer TRAMP C1 cells through epigenetic regulation. Biochem Pharmacol 85(9):1398-1404. doi: 10.1016/j. bcp.2013.02.010
16. Shen G, Xu C, Hu R, Jain MR, Nair S, Lin W, Yang CS, Chan JY, Kong AN (2005) Comparison of (?)-epigallocatechin-3-gallate elicited liver and small intestine gene expression profiles between C57BL/6J mice and C57BL/6J/Nrf2 (?/?) mice. Pharm Res 22(11):1805-1820. doi:10.1007/s11095-005-7546-8
17. Kang HJ, Hong YB, Kim HJ, Wang A, Bae I (2011) Bioactive food components prevent carcinogenic stress via Nrf2 activation in BRCA1 deficient breast epithelial cells. Toxicol Lett 209(2):154-160. doi:10.1016/j.toxlet. 2011.12.002, pii: S0378-4274(11)01653-5
18. Barve A, Khor TO, Nair S, Reuhl K, Suh N, Reddy B, Newmark H, Kong AN (2009) Gamma-tocopherol-enriched mixed tocopherol diet inhibits prostate carcinogenesis in TRAMP mice. Int J Cancer 124(7):1693-1699. doi:10.1002/ijc.24106
19. Yu S, Khor TO, Cheung KL, Li W, Wu TY, Huang Y, Foster BA, Kan YW, Kong AN (2010) Nrf2 expression is regulated by epigenetic mechanisms in prostate cancer of TRAMP mice. PLoS One 5(1):e8579. doi:10.1371/journal.pone.0008579
20. Cho HY, Reddy SP, Debiase A, Yamamoto M, Kleeberger SR (2005) Gene expression profiling of NRF2-mediated protection against oxidative injury. Free Radic Biol Med 38(3): 325-343. doi:10.1016/j.freeradbiomed.2004. 10.013, pii: S0891-5849(04)00835-4
21. Kwak MK, Wakabayashi N, Itoh K, Motohashi H, Yamamoto M, Kensler TW (2003) Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J Biol Chem 278(10):8135-8145. doi:10.1074/jbc. M211898200M211898200
22. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA (2003) Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 278(14):12029-12038. doi:10.1074/jbc.M211558200M211558200
23. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S (2004) Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 114(9):1248-1259. doi:10.1172/JCI21146
24. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 62(18):5196-5203
25. Rushmore TH, Morton MR, Pickett CB (1991) The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem 266(18): 11632-11639
26. Villeneuve NF, Lau A, Zhang DD (2010) Regulation of the Nrf2-Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxidants Redox Signal 13(11):1699-1712. doi:10.1089/ars.2010. 3211
27. Hayes JD, McMahon M, Chowdhry S, Dinkova-Kostova AT (2010) Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxidants Redox Signal 13(11):1713-1748. doi:10.1089/ars. 2010.3221
28. Yu R, Mandlekar S, Lei W, Fahl WE, Tan TH, Kong AN (2000) p38 mitogen-activated protein kinase negatively regulates the induction of phase II drug-metabolizing enzymes that detoxify carcinogens. J Biol Chem 275(4):2322-2327
29. Saw CL, Cintron M, Wu TY, Guo Y, Huang Y, Jeong WS, Kong AN (2011) Pharmacodynamics of dietary phytochemical indoles I3C and DIM: Induction of Nrf2-mediated phase II drug metabolizing and antioxidant genes and synergism with isothiocyanates. Biopharm Drug Dispos 32(5):289-300. doi:10.1002/bdd.759
30. Chen C, Yu R, Owuor ED, Kong AN (2000) Activation of antioxidant-response element (ARE), mitogen-activated protein kinases (MAPKs) and caspases by major green tea polyphenol components during cell survival and death. Arch Pharm Res 23(6):605-612
31. Wu TY, Khor TO, Saw CL, Loh SC, Chen AI, Lim SS, Park JH, Cai L, Kong AN (2011) Antiinflammatory/anti-oxidative stress activities and differential regulation of Nrf2-mediated genes by non-polar fractions of tea Chrysanthemum zawadskii and licorice Glycyrrhiza uralensis. AAPS J 13(1):1-13. doi:10.1208/s12248-010-9239-4
32. Prawan A, Keum YS, Khor TO, Yu S, Nair S, Li W, Hu L, Kong AN (2008) Structural influence of isothiocyanates on the antioxidant response element (ARE)-mediated heme oxygenase-1 (HO-1) expression. Pharm Res 25(4):836-844. doi:10.1007/s11095-007-9370-9
33. Jeong WS, Keum YS, Chen C, Jain MR, Shen G, Kim JH, Li W, Kong AN (2005) Differential expression and stability of endogenous nuclear factor E2-related factor 2 (Nrf2) by natural chemopreventive compounds in HepG2 human hepatoma cells. J Biochem Mol Biol 38(2):167-176
34. Kim BR, Hu R, Keum YS, Hebbar V, Shen G, Nair SS, Kong AN (2003) Effects of glutathione on antioxidant response element-mediated gene expression and apoptosis elicited by sulforaphane. Cancer Res 63(21):7520-7525
35. Yuan X, Xu C, Pan Z, Keum YS, Kim JH, Shen G, Yu S, Oo KT, Ma J, Kong AN (2006) Butylated hydroxyanisole regulates ARE-mediated gene expression via Nrf2 coupled with ERK and JNK signaling pathway in HepG2 cells. Mol Carcinog 45(11):841-850. doi:10.1002/mc.20234
36. Saw CL, Huang Y, Kong AN (2010) Synergistic anti-inflammatory effects of low doses of curcumin in combination with polyunsaturated fatty acids: docosahexaenoic acid or eicosapentaenoic acid. Biochem Pharmacol 79(3):421-430. doi:10.1016/j.bcp.2009.08.030
37. Chan K, Lu R, Chang JC, Kan YW (1996) NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci USA 93(24):13943-13948
38. Yoh K, Itoh K, Enomoto A, Hirayama A, Yamaguchi N, Kobayashi M, Morito N, Koyama A, Yamamoto M, Takahashi S (2001) Nrf2-deficient female mice develop lupus-like autoimmune nephritis. Kidney Int 60(4):1343-1353. doi:10.1046/j.1523-1755.2001.00939.x, pii: kid939
39. Chanas SA, Jiang Q, McMahon M, McWalter GK, McLellan LI, Elcombe CR, Henderson CJ, Wolf CR, Moffat GJ, Itoh K, Yamamoto M, Hayes JD (2002) Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochem J 365(Pt 2):405-416. doi:10.1042/BJ20020320BJ20020320
40. Cho HY, Jedlicka AE, Reddy SP, Kensler TW, Yamamoto M, Zhang LY, Kleeberger SR (2002) Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol 26(2):175-182
41. Bauer AK, Cho HY, Miller-Degraff L, Walker C, Helms K, Fostel J, Yamamoto M, Kleeberger SR (2011) Targeted deletion of Nrf2 reduces urethane-induced lung tumor development in mice. PLoS One 6(10):e26590. doi:10.1371/journal.pone. 0026590PONE-D-11-06632
42. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236(2):313-322, S0006291X97969436
43. Chan K, Kan YW (1999) Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci USA 96(22): 12731-12736
44. Yu X, Kensler T (2005) Nrf2 as a target for cancer chemoprevention. Mutat Res 591(1-2):93-102. doi:10.1016/j.mrfmmm.2005.04.017, pii: S0027-5107(05)00309-X
45. Goerttler K, Loehrke H, Schweizer J, Hesse B (1979) Systemic two-stage carcinogenesis in the epithelium of the forestomach of mice using 7,12-dimethylbenz(a)anthracene as initiator and the phorbol ester 12-O-tetradecanoylphorbol-13-acetate as promoter. Cancer Res 39(4): 1293-1297
46. Bartsch H, Nair J (2006) Chronic inflammation and oxidative stress in the genesis and perpetuation of cancer: role of lipid peroxidation, DNA damage, and repair. Langenbecks Arch Surg 391(5):499-510. doi:10.1007/s00423-006-0073-1
47. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420(6917):860-867. doi:10.1038/nature01322nature01322
48. Hussain SP, Harris CC (2007) Inflammation and cancer: an ancient link with novel potentials. Int J Cancer 121(11):2373-2380. doi:10.1002/ijc.23173
49. Ekbom A, Helmick C, Zack M, Adami HO (1990) Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 323(18):1228-1233. doi:10.1056/NEJM199011013231802
50. Boismenu R, Chen Y (2000) Insights from mouse models of colitis. J Leukoc Biol 67(3): 267-278
51. Khor TO, Huang M-T, Kwon KH, Chan JY, Reddy BS, Kong A-N (2006) Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res 66(24):11580-11584. doi:10.1158/0008-5472. can-06-3562
52. Wang H, Khor TO, Yang Q, Huang Y, T-y W, Saw CL-L, Lin W, Androulakis IP, Kong A-NT (2012) Pharmacokinetics and pharmacodynamics of phase II drug metabolizing/antioxidant enzymes gene response by anticancer agent sulforaphane in rat lymphocytes. Mol Pharm 9(10):2819-2827. doi:10.1021/mp300130k
53. Dayneka NL, Garg V, Jusko WJ (1993) Comparison of four basic models of indirect pharmacodynamic responses. J Pharmacokinet Biopharm 21(4):457-478
54. Sadikovic B, Al-Romaih K, Squire JA, Zielenska M (2008) Cause and consequences of genetic and epigenetic alterations in human cancer. Curr Genomics 9(6):394-408. doi:10.2174/138920208785699580
55. Link A, Balaguer F, Goel A (2010) Cancer chemoprevention by dietary polyphenols: promising role for epigenetics. Biochem Pharmacol 80(12):1771-1792. doi:10.1016/j. bcp.2010.06.036
56. Prendergast GC, Ziff EB (1991) Methylation-sensitive sequence-specific DNA binding by the c-Myc basic region. Science 251(4990): 186-189
57. Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9(6):465-476
58. Esteller M (2002) CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 21(35): 5427-5440
59. Hendrich B, Bird A (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18(11):6538-6547
60. Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, Bird A (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69(6):905-914
61. Feng Q, Zhang Y (2001) The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 15(7):827-832
62. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393(6683): 386-389
63. Li LC, Dahiya R (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18(11):1427-1431
64. Clark SJ, Harrison J, Paul CL, Frommer M (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res 22(15): 2990-2997
65. Grunau C, Clark SJ, Rosenthal A (2001) Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acids Res 29(13):E65-E75
66. Solomon MJ, Larsen PL, Varshavsky A (1988) Mapping protein-DNA interactions in vivo with formaldehyde: evidence that histone H4 is retained on a highly transcribed gene. Cell 53(6):937-947, pii: S0092-8674(88)90469-2
67. Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M (2007) Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods 3:11. doi:10.1186/1746-4811-3-11, pii: 1746-4811-3-11