Toward an understanding of the role of a catechol moiety in cancer chemoprevention: The case of copper- and o-quinone-dependent Nrf2 activation by a catechol-type resveratrol analog

Molecular Nutrition and Food Research

Volumn 59, Issue 12, 2015, Pages 2395-2406

  Lin, Dong ^a   Dai, Fang ^a   Sun, Lan Di ^a   Zhou, Bo ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

Cancer chemoprevention; Copper; Nrf2 o Quinone; Resveratrol

Indexed keywords

3,4'-DIHYDROXYSTILBENE; ANTINEOPLASTIC AGENT; CATECHOL; CATECHOL DERIVATIVE; COPPER; KEAP1 PROTEIN, HUMAN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; NFE2L2 PROTEIN, HUMAN; PROTEIN KINASE B; RESVERATROL; STILBENE DERIVATIVE; TRANSCRIPTION FACTOR NRF2;

CHEMISTRY; DRUG EFFECTS; HEP-G2 CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; UBIQUITINATION;

ANTICARCINOGENIC AGENTS; CATECHOLS; COPPER; HEP G2 CELLS; HUMANS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; NF-E2-RELATED FACTOR 2; PHOSPHORYLATION; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-AKT; STILBENES; STRUCTURE-ACTIVITY RELATIONSHIP; UBIQUITINATION;

EID: 84954401972     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500297     Document Type: Article

References (69)

1. Sporn, M. B., Liby, K. T., Cancer chemoprevention: scientific promise, clinical uncertainty. Nat. Clin. Prac. Oncol. 2005, 2, 518-525.
2. Steward, W. P., Brown, K., Cancer chemoprevention: a rapidly evolving field. Br. J. Cancer 2013, 109, 1-7.
3. Jeong, W. S., Jun, M., Kong, A. N., Nrf2: a potential molecular target for cancer chemoprevention by natural compounds. Antioxid. Redox Sign. 2006, 8, 99-106.
4. Yu, X., Kensler, T., Nrf2 as a target for cancer chemoprevention. Mutat. Res. 2005, 591, 93-102.
5. Jaramillo, M. C., Zhang, D. D., The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev. 2013, 27, 2179-2191.
6. Zhang, D. D., Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab. Rev. 2006, 38, 769-789.
7. Li, W., Kong, A. N., Molecular mechanisms of Nrf2-mediated antioxidant response. Mol. Carcinogen. 2009, 48, 91-104.
8. Nguyen, T., Nioi, P., Pickett, C. B., The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J. Biol. Chem. 2009, 284, 13291-13295.
9. Chen, H. D., Fu, J. S., Chen, H., Hu, Y. H. et al., Ginger compound [6]-shogaol and its cysteine-conjugated metabolite (M2) activate Nrf2 in colon epithelial cells in vitro and in vivo. Chem. Res. Toxicol. 2014, 27, 1575-1585.
10. Lin, C. Y., Chen, J. H., Fu, R. H., Tsai, C. W., Induction of pi form of glutathione S-transferase by carnosic acid is mediated through PI3K/Akt/NF-κB pathway and protects against neurotoxicity. Chem. Res. Toxicol. 2014, 27, 1958-1966.
11. Huang, H. C., Nguyen, T., Pickett, C. B., Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J. Biol. Chem. 2002, 277, 42769-42774.
12. Kumar, H., Kim, I. S., More, S. V., Kim, B. W. et al., Natural product-derived pharmacological modulators of Nrf2/ARE pathway for chronic diseases. Nat. Prod. Rep. 2014, 31, 109-139.
13. Hur, W., Gray, N. S., Small molecule modulators of antioxidant response pathway. Curr. Opin. Chem. Biol. 2011, 15, 162-173.
14. Jang, M. S., Cai, E. N., Udeani, G. O., Slowing, K. V. et al., Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997, 275, 218-220.
15. Baur, J. A., Sinclair, D. A., Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 2006, 5, 493-506.
16. Rubiolo, J. A., Mithieux, G., Vega, F. V., Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. Eur. J. Pharmacol. 2008, 591, 66-72.
17. Ungvari, Z., Bagi, Z., Feher, A., Recchia, F. A. et al., Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2. Am. J. Physiol. Heart C 2010, 299, H18-H24.
18. Kode, A., Rajendrasozhan, S., Caito, S., Yang, S. R. et al., Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am. J. Physiol. Lung C. 2008, 294, L478-L488.
19. Chen, C. Y., Jang, J. H., Li, M. H., Surh, Y. J., Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem. Biophys. Res. Comm. 2005, 331, 993-1000.
20. Cheng, A. S., Cheng, Y. H., Chiou, C. H., Chang, T. L., Resveratrol upregulates Nrf2 expression to attenuate methylglyoxal-induced insulin resistance in HepG2 cells. J. Agric. Food Chem. 2012, 60, 9180-9187.
21. Walle, T., Hsieh, F., DeLegge, M. H., Oatis, J. E. et al., High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab. Dispos. 2004, 32, 1377-1382.
22. Wenzel, E., Somoza, V., Metabolism and bioavailability of trans-resveratrol, Mol. Nutr. Food Res. 2005, 49, 472-481.
23. Wang, M. F., Jin, Y., Ho, C. T., Evaluation of resveratrol derivatives as potential antioxidants and identification of a reaction product of resveratrol and 2, 2-diphenyl-1-picryhydrazyl radical. J. Agric. Food Chem. 1999, 47, 3974-3977.
24. Fukuhara, K., Nagakawa, M., Nakanishi, I., Ohkubo, K. et al., Structural basis for DNA-cleaving activity of resveratrol in the presence of Cu(II). Bioorg. Med. Chem. 2006, 14, 1437-1443.
25. Caruso, F., Tanski, J., Villegas-Estrada, A., Rossi, M., Structural basis for antioxidant activity of trans-resveratrol: ab initio calculations and crystal and molecular structure. J. Agric. Food Chem. 2004, 52, 7279-7285.
26. Rossi, M., Caruso, F., Opazo, C., Salciccioli, J., Crystal and molecular structure of piceatannol; scavenging features of resveratrol and piceatannol on hydroxyl and peroxyl radicals and docking with transthyretin. J. Agric. Food Chem. 2008, 56, 10557-10566.
27. Farines, V., Monje, M. C., Telo, J. P., Hnawia, E. et al., Polyphenols as superoxide dismutase modulators and ligands for estrogen receptors. Anal. Chim. Acta 2004, 513, 103-111.
28. Matsuoka, A., Takeshita, K., Furuta, A., Ozaki, M. et al., The 4'-hydroxy group is responsible for the in vitro cytogenetic activity of resveratrol. Mutat. Res. 2002, 521, 29-35.
29. Stivala, L. A., Savio, M., Carafoli, F., Perucca, P., Specific structural determinants are responsible for the antioxidant activity and the cell cycle effects of resveratrol. J. Biol. Chem. 2001, 276, 22586-22594.
30. Tang, J. J., Fan, G. J., Dai, F., Ding, D. J. et al., Finding more active antioxidants and cancer chemoprevention agents by elongating the conjugated links of resveratrol. Free Radic. Biol. Med. 2011, 50, 1447-1457.
31. Shang, Y. J., Qian, Y. P., Liu, X. D., Dai, F. et al., Radical-scavenging activity and mechanism of resveratrol-oriented analogues: influence of the solvent, radical, and substitution. J. Org. Chem. 2009, 74, 5025-5031.
32. Fan, G. J., Liu, X. D., Qian, Y. P., Shang, Y. J. et al., 4, 4′-dihydroxy-trans-stilbene, a resveratrol analogue, exhibited enhanced antioxidant activity and cytotoxicity. Bioorg. Med. Chem. 2009, 17, 2360-2365.
33. Yang, J., Liu, G. Y., Lu, D. L., Dai, F. et al., Hybrid-increased radical-scavenging activity of resveratrol derivatives by incorporating a chroman moiety of vitamin E. Chem. Eur. J. 2010, 16, 12808-12813.
34. Cao, X. Y., Yang, J., Dai, F., Ding, D. J. et al., Extraordinary radical scavengers: 4-mercaptostilbenes. Chem. Eur. J. 2012, 18, 5898-5905.
35. II ions and the stilbene-chroman hybrid with a catechol moiety synergistically induced DNA damage, and cell cycle arrest and apoptosis of HepG2 cells: an interesting acid/base-promoted prooxidant reaction. Chem. Eur. J. 2012, 18, 11100-11106.
36. Zheng, L. F., Wei, Q. Y., Cai, Y. J., Fang, J. G. et al., DNA damage induced by resveratrol and its synthetic analogues in the presence of Cu (II) ions: mechanism and structure-activity relationship. Free Radic. Biol. Med. 2006, 41, 1807-1816.
37. Kang, Y. F., Yan, W. J., Zhou, T. W., Dai, F. et al., Tailoring 3, 3′-dihydroxyisorenieratene to hydroxystilbene: finding a resveratrol analogue with increased antiproliferation activity and cell selectivity. Chem. Eur. J. 2014, 20, 8904-8908.
38. Vandeputte, C., Guizon, I., Genestie-Denis, I., Vannier, B. et al., Microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biol. Toxicol. 1994, 10, 415-421.
39. Hussain, S. P., Hofseth, L. J., Harris, C. C., Radical causes of cancer. Nat. Rev. Cancer 2003, 3, 276-285.
40. Lee, H. U., Bae, E. A., Han, M. J., Kim, N. J. et al., Hepatoprotective effect of ginsenoside Rb1 and compound K on tert-butyl hydroperoxide-induced liver injury. Liver Int. 2005, 25, 1069-1073.
41. Martin, C., Martinez, R., Navarro, R., Ruiz-Sanz, J. I. et al., tert-Butyl hydroperoxide-induced lipid signaling in hepatocytes: involvement of glutathione and free radicals. Biochem. Pharmacol. 2001, 62, 705-712.
42. Hix, S., Kadiiska, M. B., Mason, R. P., Augusto, O., In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin-trapping and DNA methylation studies. Chem. Res. Toxicol. 2000, 13, 1056-1064.
43. Dinkova-Kostova, A. T., Talalay, P., Direct and indirect antioxidant properties of inducers of cytoprotective proteins. Mol. Nutr. Food Res. 2008, 52, s128-s138.
44. Jung, K. A., Kwak, M. K., The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010, 15, 7266-7291.
45. Moi, P., Chan, K., Asunis, I., Cao, A., Kan, Y. W., Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the β-globin locus control region. Proc. Natl. Acad. Sci. USA 1994, 91, 9926-9930.
46. Li, J., Johnson, D., Calkins, M., Wright, L. et al., Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells. Toxicol. Sci. 2005, 83, 313-328.
47. Lau, A., Tian, W., Whitman, S. A., Zhang, D. D., The predicted molecular weight of Nrf2: it is what it is not. Antioxid. Redox Signal. 2013, 18, 91-93.
48. Arlt, A., Sebens, S., Krebs, S., Geismann, C. et al., Inhibition of the Nrf2 transcription factor by the alkaloid trigonelline renders pancreatic cancer cells more susceptible to apoptosis through decreased proteasomal gene expression and proteasome activity. Oncogene 2013, 32, 4825-4835.
49. Greenwald, M. B. Y., Anzi, S., Ben Sasson, S., Bianco-Peled, H. et al., Can nitroxides evoke the Keap1-Nrf2-ARE pathway in skin? Free Radic. Biol. Med. 2014, 77, 258-269.
50. Zhang, D. D., Hannink, M., Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell Biol. 2003, 23, 8137-8151.
51. Lee, H. H., Park, S. A., Almazari, I., Kim, E. H. et al., Piceatannol induces heme oxygenase-1 expression in human mammary epithelial cells through activation of ARE-driven Nrf2 signaling. Arch. Biochem. Biophys. 2010, 501, 142-150.
52. Almazari, I., Park, J. M., Park, S. A., Suh, J. Y. et al., Guggulsterone induces heme oxygenase-1 expression through activation of Nrf2 in human mammary epithelial cells: PTEN as a putative target. Carcinogenesis 2012, 33, 368-376.
53. Hou, D. X., Korenori, Y., Tanigawa, S., Yamada-Kato, T. et al., Dynamics of Nrf2 and Keap1 in ARE-mediated NQO1 expression by wasabi 6-(methyl sulfinyl) hexyl isothiocyanate. J. Agric. Food Chem. 2011, 59, 11975-11982.
54. Tisato, F., Marzano, C., Porchia, M., Pellei, M. et al., Copper in diseases and treatments, and copper-based anticancer strategies. Med. Res. Rev. 2010, 30, 708-749.
55. Bystrom, L. M., Rivella, S., Cancer cells with irons in the fire. Free Radic. Biol. Med. 2015, 79, 337-342.
56. Cooper, S. R., Mcardle, J. V., Raymond, K. N., Siderophore electrochemistry: relation to intracellular iron release mechanism. Proc. Natl. Acad. Sci. USA 1978, 75, 3551-3554.
57. Fang, J. G., Lu, M., Chen, Z. H., Zhu, H. H. et al., Antioxidant effects of resveratrol and its analogues against the free-radical-induced peroxidation of linoleic acid in micelles. Chem. Eur. J. 2002, 8, 4191-4198.
58. Fulda, S., Resveratrol and derivatives for the prevention and treatment of cancer. Drug Discov. Today 2010, 15, 757-765.
59. Liu, H. C., Dong, A. J., Gao, C. M., Jiang, Y. Y., Structure modification of resveratrol and pharmacological activity. Prog. Chem. 2009, 21, 1500-1506 and references therein.
60. Yamamoto, T., Suzuki, T., Kobayashi, A., Wakabayashi, J. et al., Physiological significance of reactive cysteine residues of Keap1 in determining Nrf2 activity. Mol. Cell Biol. 2008, 28, 2758-2770.
61. Kim, S., Lee, H. G., Park, S. A., Kundu, J. K. et al., Keap1 cysteine 288 as a potential target for diallyl trisulfide-induced Nrf2 activation. PLoS One 2014, 9, e85984.
62. Mira, L., Fernandez, M. T., Santos, M., Rocha, R. et al., Interactions of flavonoids with iron and copper ions: a mechanism for their antioxidant activity. Free Radic. Res. 2002, 36, 1199-1208.
63. Sumi, D., Numasawa, Y., Endo, A., Iwamoto, N. et al., Catechol estrogens mediated activation of Nrf2 through covalent modification of its quinone metabolite to Keap1. J. Toxicol. Sci. 2009, 34, 627-635.
64. Wang, X. J., Hayes, J. D., Higgins, L. G., Wolf, C. R. et al., Activation of the Nrf2 signaling pathway by copper-mediated redox cycling of para- and ortho-hydroquinones. Chem. Biol. 2010, 17, 75-85.
65. Kim, H., Kim, W., Yum, S., Hong, S. et al., Caffeic acid phenethyl ester activation of Nrf2 pathway is enhanced under oxidative state: structural analysis and potential as a pathologically targeted therapeutic agent in treatment of colonic inflammation. Free Radic. Biol. Med. 2013, 65, 552-562.
66. Satoh, T., Kosaka, K., Itoh, K., Kobayashi, A. et al., Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J. Neurochem. 2008, 104, 1116-1131.
67. Prestera, T, Zhang, Y. S., Spencer, S. R., Wilczak, C. A. et al., The electrophile counterattack response: protection against neoplasia and toxicity. Adv. Enzyme Regul. 1993, 33, 281-296.
68. Rae, T. D., Schmidt, P. J., Pufahl, R. A., Culotta, V. C. et al., Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 1999, 284, 805-808.
69. Turski, M. L., Thiele, D. J., New roles for copper metabolism in cell proliferation, signaling, and disease. J. Biol. Chem. 2009, 284, 717-721.