Two-step mechanism of induction of the gene expression of a prototypic cancer-protective enzyme by diphenols

Chemical Research in Toxicology

Volumn 21, Issue 4, 2008, Pages 805-812

  Bensasson, René V ^a   Zoete, Vincent ^b   Dinkova Kostova, Albena T ^c,d   Talalay, Paul ^c  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; FLAVONOID; NADPH QUINONE OXIDOREDUCTASE 1; PHENOL DERIVATIVE; PROTEIN; QUINONE DERIVATIVE; THIOL GROUP;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CANCER PREVENTION; CORRELATION ANALYSIS; DRUG MECHANISM; ELECTRON; ENZYME ACTIVATION; ENZYME INDUCTION; GENE EXPRESSION; GENE INDUCTION; NEOPLASM; OXIDATION; OXIDATION REDUCTION REACTION; QUANTUM CHEMISTRY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CYTOSKELETAL PROTEINS; GENE EXPRESSION; MICE; NADPH DEHYDROGENASE; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; PHENOLS; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; REACTIVE OXYGEN SPECIES;

EID: 43149117906     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx7002883     Document Type: Article

References (47)

1. Gilbert, D. L., Ed. (1981) Oxygen and living processes, Springer Verlag, New York.
2. Halliwell, B., and Gutteridge, J. M. C. (1999) Free radicals in biology and medicine, 3rd ed., Oxford University Press, Oxford, U.K.
3. Fahey, J. W., Dinkova-Kostova, A. T., Stephenson, K. K., and Talalay, P. (2004) The "Prochaska" microtiter plate bioassay for inducers of NQO1, in Quinones and quinone enzymes, part B, Methods in Enzymology, volume 382 (Sies, H., and Packer, L., Eds.) pp 243-258, Academic Press, San Diego, CA.
4. Kensler, T. W. (1997) Chemoprevention by inducers of carcinogen detoxication enzymes. Environ. Health Perspect. 105 (Suppl. 4), 965-970.
5. Talalay, P. (2000) Chemoprotection against cancer by induction of phase 2 enzymes. Biofactors 12, 5-11.
6. Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wakabayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P. (2002) 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. U.S.A. 99, 11908-11913.
7. Dinkova-Kostova, A. T., Holtzclaw, W. D., and Kensler, T. W. (2005) The role of Keap1 in cellular protective responses. Chem. Res. Toxicol. 18, 1779-1791.
8. Motohashi, H., and Yamamoto, M. (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med. 10, 549-557.
9. Kobayashi, M., and Yamamoto, M. (2006) Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv. Enzyme Regul. 46, 113-140.
10. Kobayashi, M., and Yamamoto, M. (2005) Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signaling 7, 385-394.
11. Prochaska, H. J., De Long, M. J., and Talalay, P. (1985) On the mechanisms of induction of cancer-protective enzymes: a unifying proposal. Proc. Natl. Acad. Sci. U.S.A. 82, 8232-8236.
12. Talalay, P., De Long, M. J., and Prochaska, H. J. (1988) Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 85, 8261-8265.
13. Holtzclaw, W. D., Dinkova-Kostova, A. T., and Talalay, P. (2004) Protection against electrophile and oxidative stress by induction of phase 2 genes: the quest for the elusive sensor that responds to inducers. Adv. Enzyme Regul. 44, 335-367.
14. Scurlock, R., Rougée, M., and Bensasson, R. V. (1996) Redox properties of diphenols and their correlation to induction of enzyme synthesis. Z. Phys. Chem. 196, 85-92.
15. Zoete, V., Rougée, M., Dinkova-Kostova, A. T., Talalay, P., and Bensasson, R. V. (2004) Redox ranking of inducers of a cancer protective enzyme via the energy of their highest occupied molecular orbital. Free Radical Biol. Med. 36, 1418-1423.
16. Lee-Hilz, Y. Y., Boerboom, A. M., Westphal, A. H., Berkel, W. J., Aarts, J. M., and Rietjens, I. M. (2006) Pro-oxidant activity of flavonoids induces EpRE-tnediated gene expression. Chem. Res. Toxicol. 19, 1499-1505.
17. Pullman, B., and Pullman, A. (1963) Quantum Biochemistry, pp 128-135 and pp 495-497, Interscience Publishers, New York.
18. Hansch, C. and Leo, A. (1995) Exploring QSAR, Fundamentals and Applications in Chemistry and Biology, ACS Professional Reference Book, American Chemical Society, Washington, DC.
19. Wardman, P. (1989) Reduction potentials of the one-electron couples involving free radicals in aqueous solution. J. Phys. Chem. Ref. Data 18, 1637-1755.
20. Koppenol, W. H. (1990) Oxyradical reactions: from bond-dissociation energies to reduction potentials. FEBS Lett. 264, 165-167.
21. Koppenol, W. H., and Butler, J. (1985) Energetics of interconversion reactions of oxyradicals. J. Adv. Free Radical Biol. 1, 91-131.
22. Dixon, W. T., and Murphy, D. (1976) Determination of the acidity constants of some phenol radical cations by means of electron spin resonance. J. Chem. Soc., Faraday Trans. 2 72, 1221-1230.
23. Buettner, G. R. (1993) The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate. Arch. Biochem. Biophys. 300, 535-543.
24. Buxton, G. V., Greenstock, C. L., Helman, W. P., and Ross, A. B. (1988) Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals in aqueous solutions. J. Phys. Chem. Ref. Data 17, 513-886.
25. Land, E. J., and Ebert, M. (1967) Pulse radiolysis studies of aqueous phenol. Water elimination from dihydroxycyclohexadienyl radicals to form phenoxyl. Trans. Faraday Soc. 63, 1181-1190.
26. • radicals in aqueous solutions. Chem. Biol. Interact. 62, 227-235.
27. Marcus, R. A. (1964) Chemical and electrochemical electron transfer theory. Annu. Rev. Phys. Chem. 15, 155-196.
28. Scandola, F., Balzani, V., and Schuster, G. B. (1981) Free-energy relationships for reversible and irreversible electron transfer-processes. J. Am. Chem. Soc. 103, 2519-2533.
29. Amatore, C. (1991) Basic concepts, in Organic Electrochemistry: An Introduction and a Guide, 3rd ed., (Lund, H., and Baizer, M. M., Eds.), pp 11-119, Dekker, New York.
30. Neta, P., and Huie, E. (1990) Rate constants for reactions of peroxyl radicals in fluid solutions. J. Phys. Chem. Ref. Data 19, 413-513.
31. Wasserman, H. H., Murray, R. W., Eds. (1979) Singlet Oxygen, Academic Press, New York.
32. 2, CRC Press, Boca Raton, FL.
33. Gorman, A. A. (1992) The Bimolecular Reactivity of Singlet Molecular Oxygen, in Advances in Photochemistry, volume 17 (Volman, D., Hammond, G., and Neckers, D., Eds.) pp 217-274, John Wiley & Sons, New York.
34. Steenken S. and Neta P. (2003) Transient Phenoxyl Radicals: Formation and Properties in aqueous solutions, in The Chemistry of Phenols, Patai series: The chemistry of functional groups (Rappaport Z., Ed.), pp 1107-1152, John Wiley, Interscience Publication, New York.
35. Everse, J., Everse, K. E., and Grisham, M. B., Eds. (1991) Peroxidases in Chemistry and Biology, CRC Press, Boca Raton, FL.
36. Lambert, J. D., Sang, S., and Yang, C. S. (2007) Possible controversy over dietary polyphenols: Benefits vs risks. Chem. Res. Toxicol. 20, 583-585.
37. Sergediene, E., Jönsson, K., Szymusiak, H., Tyrakowska, B., Ivonne, M., Rietjens, and Cenas, N. (1999) Prooxidant toxicity of polyphenolic antioxidants to HL-60 cells: description of quantitative structure-activity relationships. FEBS Lett. 462, 392-396.
38. Bensasson, R. V., Jossang, A., Zahir, A., Bodo, B., and Land, E. J. (1999) Redox regulation of tumor cell toxicity by flavones from Lethedon tannaensis. Free Radical Biol. Med. 27, 95-99.
39. Neta, P., and Grodowski, J. (2005) Rate constants for reactions of phenoxyl radicals in solution. J. Phys. Chem. Ref. Data 34, 109-199.
40. Cooksey, C. J., Jimbow, K., Land, E. J., and Riley, P. A. (1992) Reactivity oforthoquinones involved in tyrosinase-dependent cytotoxicity: differencesbetween alkylthio- and alkoxy-substituents. Melanoma Res. 2, 283-93.
41. Cooksey, C. J., Land, E. J., Rushton, F. A. P., Ramsden, C. A., and Riley, P. A. (1996) Tyrosinase-mediated cytotoxicity of 4-substituted phenols: Use of QSAR to forecast reactivities of thiols towards the derived ortho-quinones. Quant. Struct.-Act. Relat. 15, 498-503.
42. Wardman, P. (1990) Bioreductive activation of quinones: Redox properties and thiol reactivity. Free Radical Res. Commun. 8, 219-229.
43. Wakabayashi, N., Dinkova-Kostova, A. T., Holtzclaw, W. D., Kang, M. I., Kobayashi, A., Yamamoto, M., Kensler, T. W., and Talalay, P. (2004) Protection against electrophile and oxidant stress by induction of the phase 2 response: Fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. U.S.A. 101, 2040-2045.
44. Dinkova-Kostova, A. T., Fahey, J. W., and Talalay, P. (2004) Chemical Structures of Inducers of Nicotinamide Quinone Oxidoreductase 1 (NQO1). In Quinones and Quinone Enzymes, part B, Methods in Enzymology, Volume 382 (Sies, H., and Packer, L., Eds.) pp 423-448, Academic Press, San Diego, CA.
45. Spencer, S. R., Xue, L., Klenz, E. M., and Talalay, P. (1991) The potency of inducers of Nad(P)H:(quinone-acceptor) oxidoreductase parallels their efficiency as substrates for glutathione transferases. Structural and electronic correlations. Biochem. J. 273, 711-717.
46. Prestera, T., Zhang, Y., Spencer, S. R., Wilczak, C. A., and Talalay, P. (1993) The electrophile counterattack response: Protection against neoplasia and toxicity. Adv. Enzyme Regul. 33, 281-296.
47. Prestera, T., and Talalay, P. (1995) Electrophile and antioxidant regulation of enzymes that detoxify carcinogens. Proc. Natl. Acad. Sci. U.S.A. 92, 8965-8969.